Follow-up care for survivors of lymphoma who have received curative-intent treatment

Review Article


Follow-up care for survivors of lymphoma who have received curative-intent treatment


J. Sussman, MD MSc*, N.P. Varela, PhD, M. Cheung, MD MSc, L. Hicks, MD MSc§, D. Kraftcheck, MD, J. Mandel, MD#, G. Fraser, MD**, L. Jimenez-Juan, MD††, A. Boudreau, RN††, S. Sajkowski‡‡, R. McQuillan‡‡


doi: http://dx.doi.org/10.3747/co.23.3265


ABSTRACT

Objective

This evidence summary set out to assess the available evidence about the follow-up of asymptomatic survivors of lymphoma who have received curative-intent treatment.

Methods

The medline and embase databases and the Cochrane Database of Systematic Reviews were searched for evidence published between 2000 and August 2015 relating to lymphoma survivorship follow-up. The evidence summary was developed by a Working Group at the request of the Cancer Care Ontario Survivorship and Cancer Imaging programs because of the absence of evidence-based practice documents in Ontario for the follow-up and surveillance of asymptomatic patients with lymphoma in complete remission.

Results

Eleven retrospective studies met the inclusion criteria. The proportion of relapses initially detected by clinical manifestations ranged from 13% to 78%; for relapses initially detected by imaging, the proportion ranged from 8% to 46%. Median time for relapse detection ranged from 8.6 to 19 months for patients initially suspected because of imaging and from 8.6 to 33 months for those initially suspected because of clinical manifestations. Only one study reported significantly earlier relapse detection for patients initially suspected because of clinical manifestations (mean: 4.5 months vs. 6.0 months, p = 0.042). No benefit in terms of overall survival was observed for patients depending on whether their relapse was initially detected because of clinical manifestations or surveillance imaging.

Summary

Findings in the present study support the importance of improving awareness on the part of survivors and clinicians about the symptoms that might be associated with recurrence. The evidence does not support routine imaging for improving outcomes in this patient population.

KEYWORDS: Lymphoma, Hodgkin lymphoma, non-Hodgkin lymphoma, follow-up, relapse

BACKGROUND

The lymphomas constitute a large group of neoplasms arising from the lymphatic system. In 2014, the Leukemia and Lymphoma Society of Canada estimated that 9000 new cases of lymphoma would be diagnosed in Canada [1000 Hodgkin lymphomas and 8000 non-Hodgkin lymphomas (nhls)], making lymphoma the 6th most common malignancy in the country1. There are many types and subtypes of nhl. Worldwide, diffuse large B-cell lymphoma (dlbcl) represents the most common subtype, accounting for 30%–40% of all newly diagnosed cases2.

Diffuse large B-cell lymphoma and Hodgkin lymphoma are considered curable with therapies that include chemotherapy, immunotherapy, and radiation; however, a significant proportion of patients will relapse, typically within the first 2 years after primary treatment. Many patients with relapse can be treated successfully for cure with salvage chemotherapy and stem-cell transplantation. For that reason, surveillance is considered important in this group to detect relapse as early as possible; the assumption is that earlier detection will lead to better outcomes by detecting subclinical disease with a lower tumour burden.

Surveillance to detect recurrence—which includes physical examination, blood tests, and imaging—is currently used to follow patients with dlbcl and Hodgkin lymphoma who are considered to be in remission after treatment. Surveillance practice, especially the frequency of imaging, is known to vary widely, and recent population studies have suggested that, in asymptomatic patients, significant over-testing can occur, without resulting in improved outcomes. Currently, no Canadian guidelines have summarized the evidence about the type and timing of surveillance testing for asymptomatic patients with dlbcl and Hodgkin lymphoma who have been treated for cure.

The intent of the present evidence summary was to assess the available evidence about the follow-up of asymptomatic survivors of lymphoma who have received curative-intent treatment. To direct the search for available evidence, 3 research questions were developed:

  • ■ Which clinical activities have been shown to be effective in detecting clinical recurrence or further hematologic neoplasms?

  • ■ What are the appropriate frequencies and timings for the clinical activities that have been shown to be effective in detecting clinical recurrence, further hematologic neoplasms, or malignancy?

  • ■ Which surveillance procedures have been shown to be effective in detecting therapy-related secondary malignancies after treatment for lymphoma?

METHODS

This evidence summary was developed at the request of the Cancer Care Ontario Survivorship and Cancer Imaging programs because of an absence of evidence-based practice documents in Ontario for the follow-up and surveillance of asymptomatic patients with lymphoma treated with curative intent. A Working Group consisting of 1 radiation oncologist, 2 hematologists, 1 regional primary care lead, 2 radiologists, 1 registered nurse, 2 patient representatives, and 1 health research methodologist from the Clinical Programs and Quality Initiatives was responsible for searching the literature, reviewing the identified evidence, and drafting the summary.

Literature Search Strategy

This literature search was conducted in two planned stages: a search for systematic reviews, and then a search for primary literature. Identified systematic reviews were to be assessed for quality using the amstar tool3 to determine whether the review could be incorporated into the present evidentiary base. Assuming that no systematic reviews were identified, a systematic review of the primary literature was also planned. If a suitable systematic review were to be found, a systematic review of the primary literature would be conducted starting from the date of the reported systematic review, with the goal of updating the evidence from the existing publication.

The Cochrane Database of Systematic Reviews, medline (Ovid), and embase (Ovid) for January 2000 to August 2015 were searched using the term “lymphoma.” Systematic reviews more than 5 years old were considered not relevant, because the main goal of the search for systematic reviews was to identify recent secondary sources covering the primary relevant literature about the follow-up care for survivors of lymphoma who had received curative-intent treatment.

In August 2015, the medline (Ovid) and embase (Ovid) databases were searched for primary literature; that search was updated in March 2016. The search strategy included the mesh term “exp lymphoma,” combined with additional terms and text words for the intervention (follow-up) and the population (survivors). The results were limited to English language articles and articles published from 2000 to 2015. Table i presents the full search strategy used to retrieve potentially relevant studies.

TABLE I Literature search strategy

 

Relevant articles were reviewed by 2 Working Group members (JS, NPV), and the reference lists of those articles were searched for additional trials. A data audit procedure conducted by an independent individual verified the accuracy of the information obtained from the studies included in this report.

Data extraction was conducted by 1 Working Group member (NPV). All extracted data and information was assessed by a second reviewer (JS) and audited by an independent individual to verify the accuracy of the information obtained from the included studies. For primary studies, key characteristics—author, year of publication, study design, study population, sample size, post-treatment follow-up protocol, and median follow-up time—were recorded. Outcomes of interest, including relapse rate, time to relapse, method of relapse detection and detection rate by follow-up activity, overall survival rate, and relapse-free survival rate, were extracted when available.

Randomized clinical trials were to be assessed for quality by examining method of randomization, reporting of blinding, power and sample size calculation, length of follow-up, reporting of details of the statistical analysis, reporting of withdrawals from treatment and other losses to follow-up, and reporting of the sources of funding for the research. Comparative, nonrandomized, and single-arm evidence was to be assessed according to full reporting of the patient selection criteria, the follow-up received by each patient, all relevant outcomes, and the source of funding.

All authors of the present report reviewed and discussed a draft, with the aim of assessing the quality of the evidence as a whole, without the use of a scoring system or cut-offs, according to the policy of the Program in Evidence-Based Care.

RESULTS

Literature Search

Of 1950 titles and abstracts identified in the search of the medline and embase databases, 1841 appeared potentially eligible on initial review, and 124 of the latter were verified to be eligible for full-text review. Of the eligible publications, eleven nonrandomized retrospective full-report studies addressed follow-up care for adult or adolescent survivors of lymphoma (or both) who had received curative-intent treatment and reported the outcome of interest (overall survival) and relapse-related outcomes (relapse detected by varying follow-up schedules, such as symptomatic versus asymptomatic relapses; relapse-free survival; median time to relapse; number of imaging tests per relapse detected). The included studies involved patients with dlbcl, lymphoid malignancies, and aggressive Hodgkin lymphoma. Table ii sets out the study and patient characteristics.

TABLE II Summary of the studies assessing follow-up care for asymptomatic survivors of lymphoma who received curative-intent treatment



 

Table iii presents a description of the study designs and the quality of the studies. Overall, the body of evidence is limited mainly by designs based on retrospective analyses of electronic medical records and by relatively small sample sizes with a low number of relapses. The sample size of the included studies ranged from a low of 109 to a high of 1221 in a population-based study comparing the survival rate of patients with lymphoma undergoing different clinical follow-up policies4,13. In most of the studies, patients had nhl5,7,8,10,1214; three studies focused on the follow-up of patients with Hodgkin lymphoma4,9,11, and one study reported on patients with both types of lymphoma6. The number of relapses ranged from a low of 15 to a high of 163 in patients with nhl10,12, and from a low of 11 to a high of 42 in patients with Hodgkin lymphoma6,11.

TABLE III Quality assessment for included studies


 

Outcomes

Clinical Activities for Detecting Recurrence

Table iv summarizes the clinical activities used for detection of clinical recurrence.

TABLE IV Clinical activities for detection of clinical recurrence or further hematologic neoplasms in asymptomatic survivors of lymphoma who received curative-intent treatment



 

Detection of Relapse:

Nine studies reported on the follow-up care of asymptomatic survivors of lymphoma who had received curative-intent treatment412. Two studies involving patients with nhl in complete remission detected a statistically significant difference in the number of relapses initially suspected by clinical manifestations (patient-reported symptoms or physical examination) compared with relapses initially suspected by imaging before clinical manifestation10,12. The study reported by Hong et al.10 assessed the role of routine imaging compared with symptom-directed unplanned early outpatient department visits in patients with dlbcl and reported that, compared with planned visits with or without clinical symptoms or signs, early visits because of symptoms or signs have a strong association with the detection of relapse (33% vs. 0.5%, p < 0.001). Similarly, the study reported by Truong et al.12 found that, for most relapses in aggressive nhl, patient-reported symptoms led to detection (86% vs. 14%, p < 0.0001).

Two additional studies in patients with nhl detected that the proportion of relapses initially suspected by clinical manifestations ranged from a low of 54%8 to a high of 78%5,7 and that the proportion of relapses initially suspected by surveillance imaging ranged from a low of 22%5,7 to a high of 46%8.

Three studies involved patients with Hodgkin lymphoma4,9,11. The study reported by Pingali et al.11 compared the incidence of relapse in patients managed with clinical surveillance alone and in those who underwent routine surveillance imaging, reporting that differences between groups were not statistically significant (7.4% vs. 3.4%, p = 0.39). The two remaining studies reported that the proportion of relapses initially suspected by clinical manifestations ranged from a low of 13%9 to a high of 64%4 and that the proportion of relapses initially suspected by surveillance imaging ranged from a low of 8%9 to a high of 27%4.

Overall Survival:

Seven studies reported on overall survival outcomes5,8,1014. Six of the studies reported comparable survival rates for patients with relapse initially detected by clinical manifestations and initially detected by surveillance imaging5,8,1114.

The study reported by Hong et al.10 found a median time from relapse to death of 6.7 months and an overall survival time of 38.3 months for 11 patients with relapse initially detected by early unplanned visits (clinical manifestations); however, determining whether routine imaging can prolong the survival of relapsed patients was not possible because of the small number of patients (n = 4) with relapse initially detected by planned visits with (n = 3) or without routine imaging (n = 1). Of those patients with relapse, the 3 whose relapses were detected at planned visits with imaging had times from relapse to death of 5.7, 7.9, and 9.0 months and overall survival times of 17.1, 18.9, and 50.2 months. For the 1 patient with relapse detected at a planned visit without routine imaging, the time from relapse to death was 7.6 months, and the overall survival time was 51.9 months.

Time to Relapse:

Four of the studies reported time to relapse7,9,11,14. Only the study reported by Lin et al.7 detected a significant benefit for patients with first presentation of relapse found by clinical manifestations than for patients with asymptomatic relapse found by surveillance imaging (mean: 4.5 months vs. 6.0 months, p = 0.042). The study conducted by Thompson et al.14 reported median times of 19 and 11 months from diagnosis to relapse in cohorts of asymptomatic patients from the United States and France respectively; the median times from diagnosis to relapse in patients with clinical manifestations of relapse were not reported. The study conducted by Dann et al.9 reported a median time to relapse of 8.6 months both for patients undergoing routine clinical follow-up and for patients undergoing routine clinical follow-up with routine imaging. Pingali et al.11 reported median times to relapse of 33 and 18 months in patients with Hodgkin lymphoma whose relapses were initially suspected by clinical manifestations and by imaging respectively.

Frequency of Imaging:

Three studies reported on frequency of imaging7,9,11. Two of the studies found that, compared with clinical surveillance, routine surveillance imaging in patients with Hodgkin lymphoma was statistically significantly associated with a higher number of scans. Dan et al.9 reported that, with routine imaging follow-up, 47.5 studies were required to detect a single relapse; clinical follow-up required 4.7 imaging studies. In the routine imaging follow-up arm, 3.9 imaging studies per patient were required; in the clinical follow-up arm, 0.6 studies per patient were required (p < 0.001). Similarly, the study conducted by Pingali et al.11 reported that the imaging rate in the routine imaging surveillance group was greater by a factor of 4.5 than the rate in the clinical surveillance group (0.89 vs. 0.21, p < 0.0001); the number of scans per relapse detected was 127 in the routine imaging surveillance arm; it was 14.6 scans in the clinical surveillance group.

No statistically significant differences by follow-up were reported in a study of patients with nhl by Lin et al.7. The average number of scans per patient was 3.2 in both the routine surveillance imaging arm and the arm in which relapse was detected by clinical manifestations (p = 0.749); the mean number of scans per year was reported to be 2.3 for routine surveillance imaging and 2.4 for clinical manifestations (p = 0.423).

Frequency and Timing of Clinical Activities for Detecting Recurrence

The literature search did not return any study specifically designed to evaluate the effectiveness of various frequencies and timings of follow-up for asymptomatic survivors of lymphoma who had received curative-intent treatment. However, the nine studies that were discussed while addressing research question 1 (effective clinical strategies) provided the follow-up schedules used by the institutions from which each population was selected and the relationship of those schedules with relapse detection (full description in Table v). Eight of the studies described follow-up schedules used by single institutions4,610,12,14. The study reported by El-Galaly et al.13 described the follow-up schedules used by two neighbouring Scandinavian countries with similar health care systems (Denmark and Sweden), but completely different traditions for routine imaging. Most studies reported performing clinical follow-up every 2–3 months for the first 2 years, and then every 4–6 months in the subsequent 3 years (years 3–5), with annual visits thereafter. Surveillance imaging was performed mainly for patients in whom relapse was suspected.

TABLE V Frequency and timing of clinical activities for detecting clinical recurrence or further hematologic neoplasms in asymptomatic survivors of lymphoma who received curative-intent treatment


 

Surveillance Procedures for Detecting Therapy-Related Secondary Malignancies

The literature search did not return any study specifically designed to evaluate follow-up schedules for detecting therapy-related secondary malignancies in asymptomatic survivors of lymphoma who had received curative-intent treatment. Documentation of therapy-related secondary malignancies might be more available in the radiation safety literature rather than in the lymphoma diagnosis and follow-up literature.

DISCUSSION

There is accumulating descriptive literature suggesting that patients with lymphoma treated with curative intent who achieve complete remission might not benefit from routine surveillance with diagnostic imaging. Currently, routine surveillance protocols, often informed by clinical trials protocols and local practice culture, include history, physical examination, blood tests, and imaging. Surveillance investigations are based on the presumption that early detection of recurrence might improve the outcomes of patients in complete remission because of a higher likelihood of successful response to salvage therapy when the clinical burden is lower. It is also recognized that certain therapies can be associated with a predictable incidence of late organ adverse effects such as heart disease or second cancers, and some routine testing is directed toward monitoring the development of such complications. In the present review, we sought to examine the evidence for surveillance and toxicity screening in this population of interest.

Currently, no Canadian consensus document sets out the optimal follow-up care for asymptomatic survivors of lymphoma who have received curative-intent treatment. The present evidence summary was framed by three areas of inquiry: clinical activities to detect relapse, frequency and timing of clinical activities to detect relapse, and activities to detect therapy-related secondary malignancies in survivors of lymphoma.

Eleven retrospective studies that specifically reported on surveillance activities to detect recurrence were identified. Complete remission was defined mainly by computed tomography imaging criteria. In most studies, a planned imaging approach, most often using computed tomography, was compared with imaging performed in response to signs and symptoms. The study populations included aggressive-histology nhl and Hodgkin lymphoma stages iiii. No prospective comparisons were found. In all studies, no significant differences in survival—our key outcome of interest—were found between planned and unplanned visits. Unfortunately, given that all nonrandomized studies carry an unclear risk of bias, the quality of the evidence supporting that summary is low.

Consistent evidence is lacking to support routine imaging surveillance in survivors of lymphoma who were treated with curative intent and who were considered to be in remission at the completion of all planned therapy. It was noted in many of the studies that, even in the planned surveillance arms, most relapses were detected in the interval between planned imaging appointments and were most often initiated by signs and symptoms reported by patients.

We also reviewed the clinical visit schedules reported in the trials. In nine studies, the timing of clinical visits was described. We were unable to find any studies that compared routine clinical visits with visits only in response to symptoms, nor any comparisons of the use of routine blood work compared with blood work at the discretion of the treating oncology team, and therefore no clinical visit schedule was described.

Most of the studies reported clinical follow-up every 2–3 months for the first 2 years, and then every 4–6 months for the following 3 years (years 3–5), with annual visits thereafter. Surveillance imaging was performed mainly in cases of suspected relapse. Most relapses are recognized to occur in the first 2–3 years after completion of therapy, and that recognition is reflected in a clinical visit pattern that is fairly consistent from study to study. The pattern is similar to that described in the 2015 National Comprehensive Cancer Network guideline15: follow-up of patients with Hodgkin lymphoma should be based mainly on interim history and physical examination; computed tomography imaging is acceptable once during the first 12 months and should be clinically prompted thereafter. Similarly, the 2015 National Comprehensive Cancer Network guideline16 for patients with nhl recommends mainly clinical follow-up, with imaging only as clinically indicated for patients with dlbcl stages i and ii, and no more often than every 6 months for the first 2 years and as clinically indicated afterward in patients with dlbcl stages iii and iv. We cannot comment specifically on the added value of blood work in surveillance testing, but other reasons to monitor blood work might be present—particularly after chemotherapy, to assess for adverse effects. Frequency and timing continue to be at the discretion of the treating oncology team.

Finally, we are unable to comment on surveillance for second malignancies in survivors of treated lymphoma because no studies specifically addressing that issue were found. We recognize that population studies describing the risks of second malignancies such as breast cancer in young women treated with chest radiation can be considered in the development of follow-up guidelines.

SUMMARY

The evidence does not support the hypothesis of improved outcomes with routine diagnostic imaging in asymptomatic survivors of lymphoma who were treated for cure and were in complete remission at the end of planned treatment.

Prospective studies are required: first, to characterize the nature of follow-up visits as they are currently practiced; and subsequently, potentially to evaluate the multiple aspects of follow-up for this patient population. Such studies should address the components of a follow-up visit that are of value from the perspective of both the health care system and the patients.

REVIEW PROCESS

This evidence summary was reviewed by the Director of the Program in Evidence-Based Care. It was also reviewed by Dr. Tom Kouroukis, Provincial Hematology Disease Site Lead at Cancer Care Ontario; Dr. Julian Dobranowski, Provincial Head of Cancer Care Ontario’s Cancer Imaging Program; Dr. Blair Macdonald, Gastrointestinal and Genitourinary Radiologist at The Ottawa Hospital; and the members of the Hematology Cancer Disease Site Group, Cancer Care Ontario. The Working Group was responsible for ensuring that the necessary changes were made.

CONFLICT OF INTEREST DISCLOSURES

We have read and understood Current Oncology’s policy on disclosing conflicts of interest, and we declare the following interests: The authors, members, and reviewers reported that they had no conflicts of interest. Nine authors declared no conflicts of interest, and two (JM, LH) declared conflicts. JM reported a potential conflict because, should lymphoma imaging indications become more liberal, his income as radiologist could potentially increase by more than $10,000. JM also declared that he had received $5,000 or more in a single year, plus other research support from Siemens, and he had been principal investigator for a clinical trial involving pet/mr studies. LH declared that she had been a co-principal investigator on a Canadian Institutes of Health Research–industry grant from Gilead Sciences. The interests as declared did not disqualify any individual from performing their designated role in the development of this evidence summary.

ACKNOWLEDGMENTS

The Cancer Survivorship Program and the Working Group thank the following individuals for their assistance in developing this report: Melissa Brouwers, Sheila McNair, Hans Messersmith, and Caroline Zwaal for providing feedback on draft versions; Julian Dobranowski, Tom Kouroukis, Blair Macdonald, and members of the Hematology Cancer Disease Site Group for reviewing the document; Elizabeth Chan for conducting data audits; and Janet Rowe for copyediting.

AUTHOR AFFILIATIONS

*Division of Radiation Oncology, Juravinski Cancer Centre, Hamilton;
Cancer Care Ontario, Program in Evidence-Based Care, McMaster University, Hamilton;
Odette Cancer Centre, Sunny-brook Health Sciences Centre, Toronto;
§Division of Hematology/Oncology, St. Michael’s Hospital, Toronto;
Provincial Primary Care and Cancer Network, Hamilton Niagara Haldimand Brant, Grimsby;
#Department of Diagnostic Imaging and Nuclear Medicine, Oakville Trafalgar Memorial Hospital, Oakville;
**Division of Malignant Hematology, Juravinski Cancer Centre, Hamilton;
††Sunnybrook Health Sciences Centre, Toronto and,
‡‡Cancer Care Ontario Patient and Family Advisor, Toronto, ON.

REFERENCES

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16. National Comprehensive Cancer Network (nccn). NCCN Clinical Practice Guidelines in Oncology: Non-Hodgkin’s Lymphomas. Ver. 1.2015. Fort Washington, PA: nccn; 2015. [Current version available online at: http://www.nccn.org/professionals/physician_gls/pdf/nhl.pdf; cited 25 August 2015]


Correspondence to: Norma P. Varela, Cancer Care Ontario, Program in Evidence-Based Care, 60(G) Wing, 2nd Floor, McMaster University, Henderson Site, 711 Concession Street, Hamilton, Ontario L8S 4L8. E-mail: Varela@mcmaster.ca

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Current Oncology, VOLUME 23, NUMBER 5, October 2016








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ISSN: 1198-0052 (Print) ISSN: 1718-7729 (Online)