• indolent lymphomas;
  • non-Hodgkin lymphoma (NHL);
  • human immunodeficiency virus-type 1 (HIV-1);
  • acquired immunodeficiency syndrome (AIDS);
  • AIDS-related NHL;
  • AIDS-related lymphoma (ARL)


  1. Top of page
  2. Abstract


There is recent evidence that the incidence of indolent non-Hodgkin lymphoma (NHL) appears to be increased in persons with the acquired immunodeficiency syndrome (AIDS). The current study was conducted to describe the clinical, immunologic, and pathologic characteristics of indolent B-cell lymphoma in patients infected with the human immunodeficiency virus (HIV).


The current report was a retrospective study of 10 cases of indolent NHL identified from the AIDS-Lymphoma Registry at the University of Southern California School of Medicine. These patients were compared with 336 consecutive patients with systemic intermediate/high-grade AIDS-related NHL who were diagnosed and treated at a single institution.


The pathology of the indolent cases included follicular lymphoma (five patients), small lymphocytic lymphoma (two patients), and one case each of mucosa-associated lymphoid tissue (MALT), monocytoid B-cell, and marginal zone lymphoma. When comparing the indolent lymphomas with the intermediate/high-grade AIDS-NHL cases, no differences were observed with regard to demographic characteristics or history of prior opportunistic infection. HIV patients with indolent lymphomas were found to have a significantly higher median CD4+ lymphocyte count compared with patients with intermediate/high-grade NHL (531 /mm3 vs. 90 /mm3) (P < 0.0001). Bone marrow involvement was significantly more common in indolent NHL cases (50%) versus intermediate/high-grade NHL cases (17%) (P = 0.02). The median survival for patients with indolent NHL was significantly longer compared with patients with intermediate/high-grade NHL (66.8 months vs. 7.1 months) (P = 0.007).


Indolent lymphomas occurring in patients infected with HIV appear to differ from intermediate/high-grade lymphomas with regard to immune status and propensity for bone marrow involvement and prolonged survival. The median survival in the group of HIV-seropositive patients with indolent NHL examined in the current study was found to be comparable to that reported in HIV-negative individuals. Cancer 2002;94:1500–6. © 2002 American Cancer Society.

DOI 10.1002/cncr.10368

Nearly 20 years have passed since the initial description of high-grade non-Hodgkin lymphoma (NHL) in patients with the acquired immunodeficiency syndrome (AIDS).1 By 1984, the association between aggressive NHL and AIDS clearly was demonstrated, and high- or intermediate-grade lymphoma became an AIDS-defining illness.2–4 Recent epidemiologic studies have estimated that the risk of developing NHL in individuals infected with the human immunodeficiency virus (HIV) is increased 150–250-fold compared with the general population.5 Moreover, the risk of lymphoma increases by 113–652-fold over that expected in HIV-infected individuals who previously have been diagnosed with full-blown AIDS.6, 7 Overall, approximately 3% of AIDS patients present with NHL,8 although as many as 16–20% eventually die of the disease.9 Although a recent international collaborative study has shown a statistically significant decline in AIDS-related lymphoma (ARL), coincident with the widespread use of highly active antiretroviral therapy,10 other studies have shown no such statistically significant decrease.11, 12 Furthermore, ARL now has become more common than some of the opportunistic infections as an initial AIDS-defining diagnosis.12

The pathologic types of ARL predominantly are high-grade (62%) or intermediate-grade (29%) B-cell lymphomas.3 More specifically, three histologic types are considered to be AIDS-defining: high-grade immunoblastic, diffuse large cell, and small noncleaved, including Burkitt or Burkitt-like lymphomas.5 Another newly described entity, primary effusion lymphoma, is associated with coinfection by HIV and human herpesvirus-8.13 Clinical, pathologic, and immunologic characteristics of these high-grade ARLs have been described previously.3, 14, 15

On occasion, HIV-infected patients have developed lymphomas of indolent histology. In a review of 90 homosexual men, Ziegler et al. reported 6 cases of low-grade NHL, comprising 7% of the group.3 Lowenthal et al. identified 3 cases of low-grade NHL among 43 patients.15 Additional case reports have included HIV-infected patients with mucosa-associated lymphoid tissue (MALT) lymphomas presenting in the gastric mucosa alone,16–18 within the lungs,19 or arising from the nasopharyngeal mucosa.20

To our knowledge, no case series to date has described the full clinical, immunologic, or pathologic characteristics of low-grade lymphoma in patients infected with HIV. This would be particularly important because a recent study that linked cancer and AIDS registries in the U.S. has demonstrated a 14-fold increase in low-grade lymphoma among HIV-infected individuals who previously were diagnosed with an AIDS-defining illness.6 To determine the clinical characteristics of indolent lymphoma among HIV-infected individuals, we evaluated our experience with 10 such patients, comparing the results with those from 336 HIV-seropositive patients with intermediate/high-grade lymphoma who were seen within the same time period at the study institution.


  1. Top of page
  2. Abstract


The AIDS-Lymphoma Registry at The University of Southern California School of Medicine includes all cases of systemic and primary central nervous system (CNS) NHL in HIV-infected patients who are diagnosed and/or managed at either Los Angeles County-University of Southern California Medical Center (LAC-USC) or the USC/Norris Comprehensive Cancer Center. From this registry, 10 patients with indolent B-cell lymphomas were identified, all of whom underwent pathologic review to confirm the diagnoses of indolent lymphoma.

All patients were determined to be HIV-seropositive by enzyme-linked immunoadsorbent assay, with confirmation by Western blot analysis. All patients had undergone an excisional biopsy or had cytologically proven NHL that was reviewed uniformly by one of us (B.N.N.). A complete history, physical examination, and routine laboratory work, including a complete blood count with differential, serum lactate dehydrogenase level (LDH), and measurements of CD4+ and CD8+ lymphocyte counts were performed at the time of diagnosis. Routine staging was performed in all patients, including computed axial tomography or magnetic resonance imaging of the chest, abdomen, and pelvis; bone marrow biopsy and aspiration; and lumbar puncture with cerebrospinal fluid (CSF) analysis. Hospital records, pathology reports, laboratory data, treatment regimens employed, responses, and survival data were reviewed and recorded.

From 1982 through September 2000, a total of 410 cases were entered into the USC AIDS-Lymphoma Registry: 362 systemic NHL cases and 48 cases of primary CNS lymphoma. A search of the database was performed to identify patients with pathologic diagnoses consistent with indolent B-cell NHL, including small lymphocytic lymphoma, MALT, follicular NHL (small cleaved, mixed, or large cell), monocytoid B-cell, lymphoplasmacytic, or marginal zone lymphoma. Twelve patients with T-cell NHL and 4 patients who were missing staging and/or follow-up data were excluded from analysis. A total of 10 cases of indolent B-cell NHL were identified, and were compared with data from 336 cases of systemic intermediate/high-grade AIDS-related NHL.

Statistical Analysis

Differences with regard to demographic, HIV, and lymphoma characteristics between the two patient groups were examined using the Fisher exact test.21 Due to unequal variance, differences in clinical laboratory data were compared using the nonparametric Kruskal–Wallis test.22 Survival time was defined as the date from the first pathologic diagnosis of lymphoma to the time of death or last follow-up, with median survival defined as the 50% point on the Kaplan–Meier curve.23 Data regarding patients who were alive or lost to follow-up were censored as of the date these patients last were seen, using a cutoff follow-up date of December 1, 2000. Differences in survival were calculated using the log-rank test.24


  1. Top of page
  2. Abstract

Patient Characteristics

A total of 10 HIV-infected patients with indolent NHL were identified. The pathologic diagnoses included follicular small cleaved lymphoma (three patients); follicular large cell lymphoma (two patients); small lymphocytic lymphoma (two patients); and MALT, monocytoid B-cell, and marginal zone lymphoma in one patient each. The group was comprised of one female and nine males. The median age of the patients at the time of diagnosis was 42 years (range, 33–57 years). Approximately 50% of the patients were Latino, whereas the remaining 50% were white. There were no significant differences between patients with indolent and intermediate/high-grade ARL in terms of demographic data (Table 1).

Table 1. Demographic and HIV-Related Characteristics
 Indolent NHLn (%)Intermediate/ high-grade NHL n (%)P value
  1. HIV: human immunodeficiency virus; NHL: non-Hodgkin lymphoma.

Median age (yrs) (range)42 (33–57)38 (21–73)0.19
 Female1 (10)15 (4)
 Male9 (90)321 (96)
 White5 (50)170 (51)
 Hispanic/Latino5 (50)131 (39)
 African-American0 (0)30 (9) 
 Asian0 (0)5 (1)
Prior Kaposi sarcoma1 (10)33 (10)1.00
Prior opportunistic infection5 (50)197 (59)0.54
Median CD4+ lymphocytes (/mm3) (range)531 (92–1927)90 (0–1466)< 0.0001
Median CD8+ lymphocytes (/mm3) (range)1161 (508–7542)551 (20–4318)< 0.0001
Median leukocyte count (×1000/mm3) (range)11.0 (1.0–27.5)4.7 (0.6–18.7)< 0.0001
Median Hemoglobin (g/dL) (range)11.8 (8.2–17)10.5 (4–17.3)0.009
Median platelet count (×1000/mm3) (range)179 (2–279)199 (5–714)0.18

HIV-Related Characteristics

Among the patients with indolent NHL, six had homosexuality or bisexuality as an HIV risk factor and two were both homosexual and intravenous drug users. One female patient had an HIV-positive male partner, and the risk factor for the acquisition of HIV in the remaining patient was unknown. One patient had a history of Kaposi sarcoma prior to lymphoma, and 5 patients (50%) had history of prior opportunistic infections. Pneumocystis carnii pneumonia was identified in three of these patients. By comparison, in 336 patients with intermediate/high-grade B-cell ARL, 10% presented with Kaposi sarcoma prior to the diagnosis of an ARL, and 60% had been diagnosed with an opportunistic infection prior to the time that lymphoma was diagnosed. The median CD4+ lymphocyte count in the patients with indolent ARL was 531/mm3 (range, 92–1927/mm3), whereas the median CD4+ lymphocyte count in the 336 patients with intermediate/high-grade NHL was 90/mm3 (range, 0–1466/mm3) (P < 0.0001) (Table 1). The median leukocyte count for the indolent NHL cases was 11,000/mm3 (range, 1000–27,500/mm3), whereas that for the high-grade cases was 4700/mm3 (range, 600–18,700/mm3) (P < 0.0001). The median hemoglobin level for indolent lymphoma patients was 11.8 g/dL (range, 8.2–17.0 g/dL), compared with 10.5 g/dL (range, 4.0–17.3 g/dL) in the patients with intermediate/high-grade NHL (Table 1).

Lymphoma Characteristics

The clinical presentation of the 10 indolent cases was not significantly different from that in the group of patients with intermediate/high-grade NHL (Table 2). Approximately 60% of the indolent NHL patients presented with “B” symptoms (fevers, drenching night sweats, or significant weight loss) compared with 66% of high-grade NHL cases. Likewise, the majority of indolent cases (70%) and intermediate/high-grade cases (66%) presented with extranodal, Ann Arbor Stage IV disease. It is of interest to note that indolent NHL patients were more likely than those with intermediate/high-grade disease to have lymphomatous involvement of the bone marrow (50% vs. 17%, respectively; P = 0.02).

Table 2. Characteristics of Lymphomatous Disease
 Indolent NHL n (%)Intermediate/ high-grade NHL n (%)P value
  • NHL: non-Hodgkin lymphoma; CSF: cerebrospinal fluid; LDH: lactate dehydrogenase.

  • a

    Normal range is 90–220 U/dL.

 I2 (20)66 (20)
 II015 (4)
 III1 (10)32 (10)
 IV7 (70)223 (66)
Extranodal sites
 Bone marrow5 (50)55 (16);2>0.02  
 CSF0 (0)35 (10)0.46  
 Liver1 (10)71 (21)0.70
 Small bowel2 (20)27 (8)0.21
 Rectum0 (0)29 (9)1.00  
 Oral1 (10)25 (7)0.55
B symptoms6 (60)214 (64)0.74
Median LDHa (U/dL) (range)225 (149–1022)280 (110–8480)0.42
Median overall survival (mos) (range)66.8 (0.2–192+)7.1 (0.1–111)0.007

Treatment and Survival

The treatment regimens given to the patients with indolent lymphoma were varied. Four patients received no chemotherapy due to poor performance status as a result of the HIV infection or the patient's wishes, and these patients survived between 0.2–18.1+ months from the time of the initial diagnosis. Chlorambucil was used in two patients, both of whom achieved a complete remission (CR). These patients lived for 13.4 months and 157.3 months, respectively, from the time of diagnosis. Another patient achieved a CR with chlorambucil, but developed a disease recurrence 10 months later. He then received combination chemotherapy with cyclophosphamide, doxorubicin, vincristine, and prednisone (CHOP), and later received cyclophosphamide, vincristine, and prednisone (CVP); the patient died of sepsis 4 years after the initial diagnosis. One patient received suramin sodium as an experimental agent in 1985, achieved a CR, and was alive at last follow-up 16 years from time of the initial diagnosis.25 A patient with follicular large cell lymphoma received multiagent chemotherapy comprised of methotrexate, bleomycin, doxorubicin, cyclophosphamide, vincristine, and dexamethasone (m-BACOD) and achieved a CR, but subsequently developed a disease recurrence and died of lymphoma 12.2 months from the time of the original diagnosis. The tenth patient with marginal zone lymphoma was alive and in CR at the time of last follow-up (29 months from the time of diagnosis) after treatment with liposomal daunorubicin.

Patients with intermediate/high-grade lymphoma received varied regimens over the years, with 48% having received low-dose or standard-dose M-BACOD and 29% having received low-dose or standard-dose CHOP. Full details have been published previously.26–28

A statistically significant difference was found with regard to survival between the patients with indolent ARL and those patients with intermediate/high-grade ARL (Table 2). The median survival for the patients with indolent NHL was 66.8 months (range, 0.2–192+ months) versus 7.1 months (range, 0.1–111 months) for those patients with intermediate/high-grade NHL (P = 0.007) (Fig. 1).

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Figure 1. Comparison of overall survival in human immunodeficiency virus-seropositive patients with indolent non-Hodgkin lymphoma (NHL) compared with patients with intermediate/high-grade (Int/High) lymphoma. The median survival for the 10 patients with indolent NHL was 66.8 months (range, 0.2–192+ months) versus 7.1 months (range, 0.1–111 months) for the 336 patients with Int/High NHL (P = 0.007)

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  1. Top of page
  2. Abstract

Indolent B-cell lymphomas represent only a small proportion of all lymphomas occurring among HIV-positive patients, accounting for < 3% of all cases in the AIDS Lymphoma Registry at the study institution. Although the demographic characteristics of the indolent cases appear quite similar to those in HIV-infected patients with intermediate/high-grade lymphoma, other characteristics of HIV disease clearly are different. Thus, patients with indolent lymphoma had a significantly higher CD4+ lymphocyte count at the time of diagnosis, with a median count of 531/mm3 versus 90/mm3 in patients with intermediate/high-grade ARL. However, despite the difference in the median CD4+ lymphocyte count, both groups had a high likelihood of opportunistic infection or Kaposi sarcoma diagnosed prior the onset of lymphoma, occurring in approximately 60–70% of both groups.

Those patients in the current study with indolent lymphoma also differed from those patients with intermediate/high-grade disease in terms of tumor characteristics. Thus, although disseminated Stage IV disease was found in approximately 70% of both patient groups, bone marrow involvement was more common in those individuals with indolent disease (50% vs. 17%; P = 0.02). Although not statistically significant, patients with intermediate/high-grade lymphoma also were more likely to present with involvement of the CSF (11% vs. 0%), liver, or rectum. As expected, patients with indolent lymphoma had lower LDH scores than those with intermediate/high-grade lymphoma.

In the current study, the median survival of the HIV-infected patients with indolent lymphoma was quite long (66.8 months), with 1 individual still alive at the time of last follow-up, 16 years from the time of the initial diagnosis of lymphoma. In contrast, patients with systemic intermediate/high-grade lymphoma had a median survival of only 7.1 months, with the longest survivor having lived approximately 9 years at the time of last follow-up (Fig. 1). The median survival of HIV-infected patients with indolent lymphoma is similar to that described in HIV-negative patients with indolent lymphomas,29, 30 with 51–74% of patients reported to be alive at 60 months from the time of diagnosis in a large study of 543 patients,29 and 66% of patients reported to have survived 5.1–7.2 years in another study of 389 patients.31 The current study data differ from those reported by Cote et al., who demonstrated that low-grade histologic type did not appear to be associated with longer survival compared with that documented in HIV-infected patients with intermediate/high-grade lymphoma.6 This discrepancy may be due to the fact that the series by Cote et al. emanated from cancer registry data, in which pathologic review was not accomplished. In the current series, all cases underwent uniform pathologic review by an experienced hematopathologist (B.N.N.). Thus, the current series of confirmed indolent lymphoma patients who were managed and treated in one institution would indicate that the median survival of these patients is significantly longer than that achieved in HIV-infected patients with intermediate/high-grade lymphoma, and quite similar to the survival times that are expected in HIV-negative patients with de novo indolent lymphoma.

The indolent ARL cases reported in the current study also shared other similarities with indolent NHLs reported to occur in the general population. Thus, both groups tend to present with disseminated disease, with Stage IV disease found to be present in 70% of HIV-infected patients in the current study versus 56% in patients with de novo low-grade lymphoma.30, 31 Bone marrow was the most common site of extranodal disease in the HIV-positive patients in the current study (reported to occur in 50% of cases), and also serves as the most common site of indolent lymphoma in HIV-negative patients, reported to occur in approximately 40–45%.30, 31

Other characteristics of indolent lymphoma among HIV-infected patients differed from those described in de novo low-grade disease. Thus, the median age of the HIV-infected patients was much younger than that of the patients with de novo low-grade lymphoma (42 years vs. 61 years).30, 31 The gender of the patients differed, with males accounting for the vast majority of HIV-infected cases, whereas males and females are reported to be distributed more equally in the HIV-negative series.30, 31 Systemic “B” symptoms appear to be quite unusual in patients with de novo low-grade lymphoma, occurring in < 33%,30, 31 whereas 60% of the HIV-infected patients were reported to present with such symptoms. Of note, these “B” symptoms may be viewed as a consequence of HIV disease as well.

Taken together, the current study data would suggest that the indolent lymphomas arising in HIV-infected patients are different from the intermediate/high-grade lymphomas in terms of characteristics of the underlying HIV disease as well as the lymphoma. Furthermore, substantially longer survival and a propensity for bone marrow involvement are reminiscent of de novo low-grade lymphoma occurring in HIV-negative patients. These data would suggest that different pathophysiologic processes may be operative in the development of indolent versus intermediate/high-grade lymphoma among patients infected with HIV. For example, more profound immunosuppression, as evidenced by low CD4+ lymphocyte counts in the peripheral blood, is believed to be a major factor in the development of intermediate/high-grade ARL, and may be predictive of the development of lymphoma in these individuals over time.12, 32, 33 Such significant depletion in CD4+ lymphocytes was not observed in HIV-infected patients with indolent lymphoma in the current study. Although underlying HIV infection may have played a role in altering certain aspects of lymphomatous disease such as lower median patient age and a higher propensity for systemic B symptoms, it is possible that these indolent lymphomas may have arisen in HIV-infected patients regardless of their HIV status.

There are several limitations to the current study. First, as a retrospective analysis, the study is subject to limitations and inadequacies of data, as well as potential patient selection bias. All patients were not treated uniformly. Furthermore, only a small number of patients were described. Nonetheless, to our knowledge the current study contains the largest group of HIV-infected patients with indolent lymphoma analyzed to date. In addition, it is clear that these cases differ from intermediate/high-grade ARLs, with median survival greater than 5 years, and disease characteristics that are very similar to those reported in patients with de novo low-grade lymphoma. It is possible that greater numbers of HIV-infected patients with indolent lymphoma will be seen in the future as the overall survival of these individuals is prolonged by the use of highly active antiretroviral therapy,34, 35 and as already suggested by matched cancer and AIDS registry data from the U.S.6


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  2. Abstract
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