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Lymphology 43 (2010) 118-127

POST-BREAST CANCER LYMPHEDEMA: INCIDENCE INCREASES FROM 12 TO 30 TO 60 MONTHS

J.M. Armer, B.R. Stewart

Sinclair School of Nursing, University of Missouri, Columbia, Missouri, USA

ABSTRACT

Breast cancer survivors are at life-timerisk of developing lymphedema (LE).Quantification of LE has been problematic asthe criteria used to identify lymphedema usevarious methods to assess changes in thevolume of the affected limb. In part because ofdifficulties and variability in measurement anddiagnosis, the reported incidence of LE variesgreatly among women treated with surgery andradiation for breast cancer. The goal of thisresearch was to describe the trends for LEoccurrence over three points in time (12, 30,and 60 months) among breast cancer survivorsusing four diagnostic criteria based on threemeasurement techniques. Participants wereenrolled following diagnosis of breast cancerbut before surgery. Baseline limb volume andsymptom assessment data were obtained.Participants were followed every 3 months for12 months, then every 6 months thereafter fora total of 60 months. Limb volume changes(LVC) in both limbs were measured usingthree techniques: objectively by (a) circum-ferences at 4 cm intervals and (b) perometryand subjectively by (c) symptom experience via interview. Four diagnostic criteria for LEmost often reported in the literature wereused: (i) 2 cm circumferential change; (ii) 200mL perometry LVC; (iii) 10% perometry LVC;and (iv) signs and symptoms (SS) report oflimb heaviness and swelling, either ‘now’ or‘in the past year’ (diagnostic criteria i-iiidefine increases/differences in limb volume

from baseline and/or between the affected andnon-affected limb). Standard survival analysismethods were applied to identify when thecriteria corresponding to LE were met. Trendsin LE occurrence are reported for preliminaryanalysis of data from 236 participantscollected at 6-, 12-, 18-, 24-, 30-, and 60-months post-op. At 60 months post-treatment,LE incidence using the four criteria rangedfrom 43% to 94%, with 2 cm associated withthe highest frequency for lymphedemaoccurrence and SS the lowest. Sixty-monthtrends are compared to earlier trends at 12-and 30-months, per criterion. These prelimi-nary findings provide additional evidence thatbreast cancer survivors are at risk fordeveloping LE beyond the first year followingtreatment. Cases of lymphedema continue toemerge through 60-months post-breast cancersurgery. This 60-month analysis supports theprevious 12- and 30-month analyses in findingthe 2 cm criteria to be the most liberal defini-tion of LE. The self-report of heaviness andswelling, along with 10% LVC, represent themost conservative definitions (41% and 45%,respectively). Furthermore, the variety ofcriteria used to identify LE, along with theabsence of baseline (pre-treatment) measure-ments, likely contribute to the wide range ofLE incidence rates reported in the literature.

Keywords: breast cancer, secondarylymphedema, diagnostic criteria (forlymphedema), lymphedema occurrence,survival analysis (for lymphedema)

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Nearly 200,000 American women arenewly affected by breast cancer each year and it is the most common type of women’scancer in the U.S., accounting for 27% of allcancers (1). Breast cancer comprises the mostcommon cancer for women (outside of skincancer) in developed parts of the world (2).Worldwide, more than a million women arenewly diagnosed with breast cancer everyyear, accounting for one tenth of all newcancers and nearly one-quarter (23%) of allfemale cancer cases (2). In addition, almost2.5 million breast cancer survivors are livingin the U.S. (1), and the five-year survival ratein Europe is 76% (3). Of those affected bybreast cancer, it is conservatively estimatedthat up to 40% will develop lymphedema(LE), depending on criteria applied. However,all survivors are at risk for developing LEover their lifetime (4,5), and the number ofsurvivors affected and potentially affected bysecondary LE is staggering, comprisingpotentially 1 to 5 million people.

Lymphedema is the accumulation ofprotein-rich fluid in the interstitial spaces ofthe affected body part due to a blockage ormalfunction in the lymph system. This edemais different from post-op swelling which mayoccur immediately after surgery. LE swellingmay cause discomfort and sometimesdisability; additionally, it can lead to cellulitisand lymphangitis, predisposing the patient tosystemic and sometimes life-threateninginfection. The physical and psychologicalaspects of the condition greatly impact thedaily lives of LE patients (6-10). Indeed,research has shown even minimal limbvolume increase affects quality of life (10). An increasing number of studies report onrisk factors related to the development ofsecondary LE, including body weight (11),and type of surgery, body weight, infection,and injury (12). Co-morbidities of elevatedBMI, orthopedic issues, cardiac conditionsrequiring medication usage, and cancerstaging requiring hormone blocker usage werealso found more often in those with LE (13).

Recent scientific literature reports that

anywhere from 5 to 60 percent (14) or 6 to62.5 percent (15) of the breast cancerpopulation meets the criteria for LE. Medicalliterature, however, suggests a more conser-vative occurrence, 15 to 20 percent of thebreast cancer population (16). A commonestimate is that 20 to 40 percent of breastcancer survivors develop LE (7,17-21), andthe rate does not significantly vary betweenCaucasians and African-Americans (22). Thediscrepancies among the reported percentagesstem from difficulties in measurement,diagnosis, and follow-up (14,15,21,23-27) aswell as the lack of pre-operative baselinecomparison or adjustment for changes inbody mass index (BMI).

Traditionally, finding 2 or more cmdifference in limb girth at some anatomicpoint between the affected and non-affectedlimbs warranted clinical diagnosis of LE (25-28). However, other methods are alsocommonly used. A 200 ml limb volumedifference or a 10 percent limb volumechange (LVC) from baseline and/or betweenthe affected and non-affected limb are bothdocumented methods of LE diagnosis (25-27,29). Self-reported signs and symptoms arealso identified as predictive of LE (25-27,30).Recently, a novel BMI-adjusted criterion was used to assess LE occurrence (31).

The reported incidence of LE fluctuatesgreatly among each participant group at riskfor LE. It has been found that often breastcancer patients do not recall being madeaware of the risk of LE post-op (32,33). Thislack of information may cause them to takelonger to recognize and report possiblesymptoms of LE. Likewise, some survivorsmay not report symptoms because they maynot know what LE is or how to detect it (32)or they were unaware of swelling (34). Othersurvivors are well-aware of their risk anddetect LE via self-assessment. However,overall a lack of sufficient knowledge aboutLE and its effects contributes to variance insurvivors’ reported incidence of LE. Healthcare providers do not typically report data onLE occurrence to a central data bank so


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epidemiological evidence of LE occurrence isfragmented.

While numerous studies have reportedLE incidence during the first 12 monthsfollowing breast cancer treatment, little isknown regarding long-term LE occurrence.Very few studies have examined LE incidencepast one year post-surgery, and many thathave are retrospective or cross-sectional, notprospective, in nature. In fact, in one analysisof existing literature, the authors found thestudy with the shortest follow-up (12 months)reported the lowest LE incidence (14). Like-wise, the study with the longest follow-up (11years) reported the highest incidence (14). Itis also reported that chart-review of medicaldiagnosis frequently understates the trueincidence of LE (35), a finding corroboratedin our current research (unpublished data).

AIMS

The current study aimed to comparethree measurement techniques using fourdiagnostic criteria to quantify LE occurrenceup to 60 months post breast cancer surgery.Trends for LE occurrence were examinedover three points in time (12, 30, and 60months). This study is unique in its prospec-tive design, examining LE prevalence through 5 years with baseline data collectionoccurring before and immediately followingsurgery. The preliminary findings will addnew insight into late-onset lymphedemaemergence and the rationale for the durationand measurement approach for optimalobservation of LE incidence.

METHODS

The study was designed to use prospec-tive, repeated-measures on data collected on236 female participants newly-diagnosed withbreast cancer. Participant recruitment anddata collection took place at a Midwesternuniversity-affiliated state cancer center. Theparticipants were consented, enrolled, andassessed at pre-diagnosis, post-surgery, every

3 months for 12 months, then every 6 monthsthereafter for a total of 60 months.

Two objective measurement techniqueswere used at each visit to quantify limbvolume characteristics: circumferentialmeasurement and infra-red perometery. (A)Traditional anthropometric measurementsrecorded limb girth every four cm on eacharm using a non-stretch, flexible tapemeasure. (B) Infra-red perometry (Perometer350S, Juzo, Cuyahoga Falls, OH) was used torecord three-dimensional images of eachlimb, which were the basis for limb volumecalculations. Both upper limbs weremeasured at each time point for comparison,with the mean of three repeated measuresused in the analyses. A detailed description of these techniques has been previouslypublished (25-27).

In addition to the two objective measures,one subjective assessment of LE symptomswas administered each visit through a nurseinterview using the LE and Breast CancerQuestionnaire (LBCQ) as a guide. The LBCQconsists of 57 questions examining 19 signsand symptoms drawn from the literature andclinical observation and has been validatedpreviously (30). Based on these publishedfindings, self-report of heaviness or swelling‘now’ or ‘in the past year,’ was included asone definition for LE.

From those measurements, four criteriafor identifying LE were used: (i) 2 cmcircumferential change at any measuredanatomic location; (ii) 200 mL perometrylimb volume change (LVC) in the affectedarm; (iii) 10% perometry LVC in the affectedarm; and (iv) report of limb heaviness andswelling, either ‘now’ or ‘in the past year.’The objective-based criteria for identifyingLE (items i-iii) were based on change frombaseline measurements and/or versuscontralateral unaffected limb.

Certain participants met the definitionsfor LE before surgery at the baselinemeasurement for one or more of the four thecriteria used here. Data from those partici-pants were retained in the study but were not


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included in the analysis for that particularcriterion, resulting in different numbers ofparticipants for a given criterion. A subjectwho met the definition at one time point wasconsidered to have met the definition at allsubsequent time points.

Sample Description

At enrollment in the study, the mean ageof participants was 57 years old (range 30 to89). The treatment characteristics of studyparticipants varied greatly. The majority ofthe participants, 48 percent, had a mastec-tomy, 39 percent had a lumpectomy, and 11 percent had both surgical treatments.Sixty percent underwent chemotherapy and51 percent underwent radiation treatment.Forty-three percent of participants hadsentinel lymph node biopsy (SLNB) treat-ment, and 30 percent underwent axillarylymph node dissection (ALND). Elevenpercent underwent both SLNB and ALNDtreatments while 16 percent had neithertreatment. All of these treatment charac-

teristics illustrate the diverse yet represen-tative treatment of the study sample.

Survival Analysis

The Lifetest procedure in SAS v9 (SASInstitute Inc., Cary, NC, USA) was used toestimate the survival distributions under eachof the definitions of LE using the product-limit or Kaplan-Meier method. Survivalanalysis allows one to estimate the probabilityof distribution of time to a specified event.Specifically, the survival curve gives theprobability that the event of interest willoccur later than a given time. The event ofinterest in this analysis is the diagnosis of LE.At time 0 (baseline), the probability is 1.00 (or 100%) that no one has met the criteria fordiagnosis. Time was measured from initialbreast cancer treatment (surgery) to the firstdiagnosis of LE. Kaplan-Meier estimates ofthe survival curves were obtained separatelyfor each of the four definitions of LE and aredisplayed in Fig. 1.

Fig. 1. Comparison of four methods for estimating lymphedema using observations from baseline to 60 months postsurgery and survival analysis.


TABLE 1Occurrence Rates of Lymphedema Using Four Diagnostic Criteria

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For any subject for whom the LE diag-nosis was met, the actual time is not knownprecisely since limb volume was measuredevery 3 months for the first year and thenevery 6 months to 60 months, and not everyday. When present, we know LE occurredsince the previous measurements were takenbut we do not know precisely when itemerged. Further, although subjects werescheduled for measurement visits at 3 or 6month intervals, the actual time betweenvisits varied (27).

Limitations

Only data from subjects with pre-opbaseline measurements were used in thisanalysis. Also, immediate post surgery data,which may provide insight to the earliestpossible onset of LE, was excluded fromanalysis due to potential confounding resultsfrom post surgery swelling. Thus, theimmediate post-op visit data were omitted forall four survival analyses to avoid mistakenlyidentifying post-op swelling as LE. Somesubjects met the definition of lymphedemawith comparisons made only to the ipsilaterallimb at baseline and not to the contralateral

limb at a particular time point. Although thismay not appear to take into account changesin body mass, we have previously shown inthis cohort that the comparisons to either the ipsilateral or contralateral limb are notsignificantly different (10). In addition, pre-liminary analysis using BMI-adjusted valueshave not affected the trends in the slope ofthe curve (manuscript in progress). We alsoconsidered a subject who met the definition of lymphedema at one time point to meet thisdefinition at all subsequent time points. Thismay increase the reporting of lymphedemabut it reflects current clinical care. It alsoprotects against misleading conclusions fromsubjects who undergo treatments that reducethe size of their limb and therefore would nolonger meet the definition of lymphedema atsubsequent time points.

RESULTS

The 2 cm identifying criterion was themost liberal of the four methods examinedhere, resulting in the highest estimation of LEat the end of the 30 months (87%) and at 60months (94%). The 200 mL LVC criteria wasthe second most likely to identify LE at the


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end of 30 months (65%) and at 60 months(83%). Meanwhile, 10% LVC and SS were themost conservative of the criteria, identifyingLE in 50% and 43% of the participants at 60months, respectively. The lymphedemaincidence rates for each method over time(each six-month interval from baseline tosixty-months) are presented in Table 1. Inaddition, the survival analysis is displayed inFig. 1 for all four criteria at 60 months. Figs.2 to 5 display the survival analyses forpreliminary exploration of trends at 12 and30 months alongside the 60-month analysisreported here. Each of the four criteria isseparately displayed. These sequentialanalyses performed as larger numbers ofsurvivors were enrolled and followed overtime provide increased confidence in thetrends seen.

When examined over smaller timeframes, the overall trends continued. At any6-month point of time during the study, the 2cm criteria identified participants with LE atthe highest frequency. Similarly, 200 mL LVCwas the second most likely to identify LE atany point in the study. However, while 10%

LVC and SS had similar occurrence rates at30 months, they had somewhat different ratesof LE emergence over that time period. SSwas more likely to identify LE in the first 12months (32%), then slowed (36% at 30months and 43% at 60 months). In contrast,10% LVC was slower to identify LE (22%) inthe first 12 months, but relatively doubled the rate of identifying LE thereafter (40% atmonth 30 and 55% at month 60).

DISCUSSION

Previous work in our laboratory hasshown that identification of LE in the firstyear post-surgery for breast cancer variesgreatly depending on the four commonly-used criteria for defining LE (26). Thesefindings were further corroborated in the 30-month analysis (27). The present studyexpands on these findings by measuring LEoccurrence through five years, one of the onlybodies of work to prospectively measure LEoccurrence for that length of time. As withthe 12- and 30-month findings, LE incidencevaried greatly depending on the criteria used.

Fig. 2. Survival analysis for 2 cm criteria to identify LE based on three different points of time.


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Fig. 3. Survival analysis for 200 mL LVC to identify LE based on three different points of time.

Fig. 4. Survival analysis for 10% LVC to identify LE based on three different points of time.

Nearly all participants (94%) met the criteriafor LE based on the 2 cm method, by far thehighest incidence rate in this analysis. Incontrast, SS identified the fewest participants(43%). This wide range of occurrence rates(51%) mirrors the high and low range ofoccurrence rates at 12 months (66% to 22%

using 2 cm and 10% LVC, respectively). This finding represents a common situation,since in the absence of a “gold standard” todiagnosis LE there exists a wide range ofcriteria used by nurses, therapists, physicians,and researchers. This analysis providesevidence that the discrepancies widely noted


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in the literature regarding the identificationof LE are due, in part, to the variety ofcriteria used.

A unique aspect of the design of thisstudy is the use of pre-surgery measurementsas baseline data. The majority of the litera-ture available is based on LE occurrenceusing post-treatment data as the comparisoncriteria. By using pre-surgery measurements,we were able to identify those participantswho met the criteria for, but did not have,lymphedema at baseline. Those participantswere not included for further analysis for thatparticular criterion, eliminating a confoundingfactor for later LE identification. Using thismethod, up to 23% of the participants atbaseline were identified to meet one of thecriteria for LE before treatment due toreasons other than LE (i.e. limb volumedifferences due to arm dominance). It is theobjective measurements (2 cm, 10% LVC, 200 mL LVC) that were the criteria morefrequently met (11-21%), while the subjectivecriterion (SS) was met at pre-surgery muchless frequently (7%). The lack of pre-surgerymeasurements in other studies likely resultsin erroneous (under-) estimation of LE, and

contributes to the wide-ranging discrepanciesin LE occurrence rates across the literature.These findings document the importance ofpre-treatment anthropometric and symptomdata collection.

These preliminary findings provideadditional evidence that breast cancer sur-vivors are at a long-term risk for developingLE. Indeed, our findings show that LEemergence, regardless of the method used forestimation, continued to increase past thefirst year post-treatment. From month 12 tomonth 30, LE identification increased by anadditional 4-25%, and from months 30-60, LE incidence increased by 7-18%, dependingon the criterion used. This increase thatoccurs past the first 30 months underscoresthe need for long-term surveillance measure-ment of limb volume and patient signs andsymptoms in breast cancer survivors byhealthcare professionals.

The preliminary results of this 60-monthanalysis of LE occurrence provide uniqueinsight into one aspect of breast cancersurvivorship. Future research in our programof study will continue to examine LE inci-dence up to seven years post-breast cancer

Fig. 5. Survival analysis for signs and symptoms to identify LE based on three different points of time.


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treatment. In addition, a prospective longi-tudinal risk-reduction intervention for thetreatment and management of LE is currentlyunderway. Thirdly, a psychosocial analysis ofthe impact of breast cancer, an equallyneglected area of LE research, is ongoing.Finally, a pilot study examining geneticpredisposition for development of secondaryLE among breast cancer survivors is under-way. These and other work now underwayhold promise in increasing our understandingof lymphedema risk factors and emergencefollowing breast cancer treatment.

CONCLUSIONS

Confirmation of the 12- and 30-monthLE trends at 60 months increase ourconfidence in the findings. These preliminaryfindings provide additional evidence thatbreast cancer survivors are at a risk fordeveloping LE beyond the first year followingtreatment. This 60-month analysis supportsthe previous 12- and 30-month analyses infinding the 2 cm criteria as the most liberaldefinition of LE. The self-report of heavinessand swelling, along with 10% LVC, representthe most conservative definitions (43% and55%, respectively) at 60 months. Further-more, these analyses demonstrate that therange of criteria used to identify LE, alongwith the lack of pre-treatment measurements,are likely responsible for the wide range oflymphedema rates reported in the literature.

ACKNOWLEDGMENTS

The statistical assistance of Dr. RichardMadsen and Isabella Zaniletti is gratefullyacknowledged. The authors would like tothank Ellis Fischel Cancer Center clinicalcollaborators, the lymphedema researchproject team, and the breast cancer survivorswho participated in the study.

The data for this project were supportedby Grant Numbers 1 R01 NR05342-01 and 1 R01 NR010293-01 from the NationalInstitute for Nursing Research, National

Institutes of Health; MU PRIME MU PRIMEfund # PRM-01-007, University of Missouri;and Ellis Fischel Cancer Center research giftfunds. The contents of this manuscript aresolely the responsibility of the authors and donot represent the official views of theNational Institutes of Health or theUniversity of Missouri.

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Jane M. Armer, RN, PhD, FAAN, CLT/MLDProfessor, Sinclair School of NursingS312 School of Nursing BuildingDirector, Nursing Research, Ellis Fischel

Cancer CenterDirector, American LymphedemaFrameworkProject DC 116.05 Suite 408 EFCC University of MissouriColumbia, MO 65211Telephone: (573) 882-0287Fax: (573) 884-4632 (notify)Email: [email protected]


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