Assessment tools for chemotherapy-induced peripheral neuropathy: a narrative review of clinician, patient-reported, and objective measures.

Introduction

Chemotherapy-induced peripheral neuropathy (CIPN) is a prevalent and debilitating side effect of cytotoxic cancer treatments leading to impairments in motor, sensory, and autonomic function. 1 While the exact pathophysiology of CIPN is poorly understood, potential mechanisms include neuroinflammation and electrophysiological disturbances. 2 Chemotherapy-induced peripheral neuropathy symptoms arise typically concurrently with chemotherapy or within weeks after completion of chemotherapy, with prevalence within the first month being upwards of 68%. 3 For many patients, CIPN symptoms decrease or resolve in the first 3-6 months from chemotherapy completion. 4 However, CIPN can persist for several months or be permanent depending on the chemotherapeutic agent, dose, duration, and patient profile. 4 , 5

Patients with CIPN can exhibit both sensory or motor symptoms that can be either “positive” (eg, pain) or “negative” (eg, loss of sensation). 6 At a sensory level, neuroinflammation leaves patients with altered skin sensations such as pain, numbness, burning, and tingling. 7 Motor neuropathy features loss of muscle strength, reflexes, and can lead to muscle atrophy. 8 Although most neuropathies from CIPN are sensorimotor, autonomic neuropathies may also arise, leaving patients with incontinence, constipation, or sexual dysfunction. 8 All types of CIPN symptoms have quality of life implications and can lead to impairments in social and vocational functioning. 7 , 9 Moreover, loss of sensation and/or strength in the lower limbs can lead to gait instability and patients with CIPN have a ∼2.5 times higher risk of falls than cancer patients without CIPN. 7 , 10

Tools to measure CIPN are needed both clinically and for research purposes. A challenge with assessing CIPN is the multifaceted nature of its symptoms requiring comprehensive forms of measurement to diagnose, monitor, and provide personalized treatment. 9 Current measurement approaches consist of patient-reported outcome measures (PROMS), clinician-based grading scales, as well as a variety of objective approaches. PROMs provide meaningful measures of CIPN which account for the patient perspective, with questionnaires including domains centering on symptom severity, quality of life and/or functional impact. Clinician-based grading scales are used by clinicians to classify patients based on their symptom severity, as classification of patients can provide a basic understanding of CIPN status that can be communicated across circles of care. Objective measurement tools offer high sensitivity through the use of specialized tools to assess patient nerve conduction, reflexes, and pain sensation. Each assessment approach has strengths and weaknesses to consider when selecting the optimal tool.

The purpose of this narrative review was to examine the practical factors, strengths, and drawbacks of current CIPN measurement tools used in various means of assessment. This review will provide a broader scale analysis of a variety of tools, providing greater breadth that may be useful for researchers and clinicians. This includes interpretability through scoring or minimum clinically important differences (MCIDs), considerations of accessibility, feasibility (duration, language, equipment training, cost, and licensing), validity and reliability. The aim is to provide clinicians and researchers with a comprehensive overview of the measurement tools available so they can select ones that best suit their clinical/research goals and available resources.

Methods

This review followed the Scale for the Assessment of Narrative Review Articles (SANRA) methodology guidelines. 11 The SANRA scale comprises 6 items to ensure a structured and rigorous approach to synthesis and quality assessment of the literature. 11 First, justification of the article’s importance seeks to highlight the value the article can bring to the readership. 11 Second, a statement of specific purpose/aims should be proposed so as to structure the direction of the review. 11 Third, a description of the literature search strategy should be outlined, mentioning search terms and types of articles included. 11 Fourth, referencing should be present for all key statements. 11 Fifth, scientific reasoning and evidence should be provided for key arguments. 11 Finally, data should be presented in a way that appropriately complements and supports the central topic of the review. 11

Literature search strategy

Studies describing CIPN measures were identified by 2 investigators through a comprehensive search of major medical and scientific databases, including PubMed and MEDLINE, using predefined search terms related to CIPN and CIPN-specific subjective and objective measurement tools (eg, CIPN measurement, CIPN questionnaire). No date restrictions were applied. In addition to keyword searches, references were also traced back from key articles. To enhance the robustness of our review, we included CIPN measurement tools listed from existing systematic reviews, while compiling other tools identified in the literature.

Measurement tools were included if they met the following criteria: (1) tools that have been used in adults with CIPN (in research or clinical practice), rather than noncancer attributable neuropathy, (2) provided measurements specific to neuropathy (rather than physical or overall function), (3) were a novel measurement system (as opposed to a compilation of previously established measures), and (4) were intended to assess neuropathy either during or after completion of chemotherapy. We searched for and included the primary articles reporting on the development and psychometrics of these tools.

Data extraction

Data were extracted on assessment type (PROMs, clinician-based grading scales, or objective measures), measurement characteristics (eg, duration, number of items), validity, reliability, MCID, and domains assessed (eg, sensory/motor/autonomic neuropathy, quality of life). Ease of use was determined depending on the amount of training, assistance, or materials required. PROMs were considered “easy” if little to no outside assistance was required and the questionnaire could be self-administered. Objective measures were considered “easy” if they required little to no training to be run and required 10 min or less to complete and “hard” if they required more extensive training prior to administering and required 15 min or more to complete. Measures were classified as subjective or objective, with subjective measurement tools having 2 subcategories; PROMs and clinician-based grading scales. Data were extracted from source papers and any available appendices. If information was not available, we did not contact study authors, as we sought to uphold the importance of publicly available information. Any missing information was indicated as “NA” in our results. Data extractions were performed by one study author (K.C.), and measures were cross-checked by a second study author (E.A.).

Data analysis

Data were reviewed and summarized through counts and reviewed qualitatively for general patterns. Finally, discussions with the research team and subject matter experts were undertaken to identify potential gaps and ensure a comprehensive analysis of the topic.

Results

Subjective measurement tools

Clinician-based grading scales

We identified 3 common clinician-based grading scales for CIPN ( Table 1 ). Two other measures, Eastern Cooperative Oncology Group Performance Status Scale and Karnofsky Performance Status were identified but excluded, given their focus on overall patient function and performance status rather than neuropathy. Each of the 3 identified tools had grading scales numbered from 0 to 4, with 0 indicating normal function and 4 indicating complete paralysis or sensory loss. Each scale assessed multiple domains of neuropathy, with the World Health Organization Chemotherapy-Induced Peripheral Neuropathy Criterion (WHO CIPN) being the only one to specifically assess all 3: sensory, motor, and autonomic.

Patient-reported outcome measures

We identified 20 PROMs used to assess CIPN ( Table 2 ). 38 , 42 , 43 , 45 , 47 , 48 Common domains assessed included sensory and motor neuropathy as well as neuropathic pain, and roughly half assessed patient quality of life. Out of the 20 PROM tools, 16 have established validity and reliability in CIPN populations and 5 have established MCIDs. One tool had established validity but not reliability. Most PROMs take 15 min or less to complete and are easy/accessible to use with no external assistance required. Scoring differs widely between PROMs due to variance in the number of items and format of the questions. Four PROMs require licensing, though some of these are free for academic use. Eleven PROMs had multiple language options such as English, Chinese, and French. Some notable PROMs that are more well established and used more often in the literature include the Functional Assessment of Cancer Therapy/Gynecologic Oncology Group-Neurotoxicity (FACT/GOG-Ntx), European Organization for Research and Treatment of Cancer Quality of Life Chemotherapy-Induced Peripheral Neuropathy Questionnaire (EORTC QLQ-CIPN20), and the National Cancer Institute Patient-Reported Outcome Common Terminology Criteria for Adverse Events.

Objective measurement tools

A total of 8 objective measures for CIPN were identified ( Table 3 ). Objective measures of CIPN are commonly used as a core standard in clinical practice to assess and monitor CIPN in patients 65 and have high sensitivity. 66 They are used less often in research as they typically require specialized equipment and training, resulting in low feasibility. 66

Of the 8 measures, 3 have been validated in CIPN populations, 12 , 20 , 58 2 have been validated in diabetic neuropathy, 49 , 60 and 1 in nerve injured patients when testing sensation in the hands. 51 The remaining 2 have not been validated. 49 , 63 Domains assessed in these measures included overall sensation, muscle strength, reflexes, sense of position, pain sensation, vibration sensation, temperature sensation, and electrical activity. The majority of assessments ( n = 5) require 10 min or less to complete, while the others ( n = 3) require 15 min to an hour. Only 3 measures have an established MCID, 1 in CIPN and 2 in other populations. 53 , 55 , 57 Of the remaining 5 measures, 3 have clinical thresholds based on binary scoring, and 2 have no established MCID or threshold.

It is also important to note that although all of these objective measures have been tested or used in CIPN populations, none were originally developed for CIPN assessment; 4 were developed or most commonly used for diabetic neuropathy, 49 , 54 , 61 , 67 1 for trauma-induced nerve injury, 68 1 for carpal tunnel syndrome, 51 1 for immune-mediated polyneuropathies, 58 and 1 as an objective measurement of pain or sensation. 63

All 8 of the objective measures require specialized equipment. Seven require some form of training, with 5 requiring minimal amounts of training including standard review of operating procedures and/or general training from someone who has completed the assessment before. Nerve conduction studies (NCS) and quantitative sensory testing require extensive training such as completing a course or program, gaining practical experience, and registering with an organization.

Discussion

In this narrative review of CIPN measurement tools, 3 clinician-based grading scales, 20 PROMs and 8 objective measures were identified. While a majority of these measurement tools are validated (as described in Tables 2 and 3 ), a minority of them have MCIDs. Most PROMs are easy to use, accessible with little training required, and assess sensory and motor domains of CIPN; approximately half assess quality of life. Conversely, most objective tools only assess the sensation domain and are less accessible due to time and training requirements to use.

Clinician-based grading scales provide standard classifications for the level of patient CIPN severity that can be communicated across and within circles of care. However, challenges arise assessing the level and/or individual impact of “severity”. Although a clinician may provide a certain grading of severity, each individual patient may have a different experience, perception, and/or impact of this severity. 69 For example, pain tolerance and impact on function may differ between individuals with different social/vocational goals (eg, a pianist or a mechanic, compared to an accountant). There lacks a consensus on whether severity should be determined through signs and symptoms, through degree of functional impairment, or a combination of both. 69 In addition, prior studies have found that clinician-based grading scales show high interobserver variability, low sensitivity to change, and underestimation of severity. 69 , 70 As such, though clinician-based grading scales may be useful for communicating certain aspects of CIPN severity, comparison across clinical situations, and in clinical trials, they do not provide a comprehensive assessment. 69 Additional forms of measurement in different domains and/or consideration for repeated measurements are likely required to provide a more comprehensive assessment.

Patient-reported outcome measures provide a more individualized and patient-centric approach toward understanding the effects and impact of CIPN. In addition to assessing severity of neuropathy, some PROMs identified also included assessment of quality of life, emotional well-being, and functional capability, providing a more comprehensive understanding of the patient’s perspective ( Table 2 ). A recent study found that certain PROMs were able to discriminate between CIPN severities better than objective measures—these included the 2 PROMs we identified with established MCIDs: the FACT/GOG-Ntx and the EORTC QLQ-CIPN20. 71 These 2 PROMs are used widely, well developed, and validated. Patient-reported outcome measures are also a fast, easy, and accessible way to gather patient data. However, certain limitations with PROMs do exist, such as lack of a “gold standard” and lack of validation in culturally diverse populations. Many PROMs identified in this review were developed and validated in a specific region or group of individuals, leading to some uncertainty about their external validity in individuals with different ethnic, cultural, or geographic backgrounds. Certain aspects of CIPN, such as pain or functional capacity, may be expressed/considered differently in different cultures. 72 While a large number of PROMs exist, the selection of a PROM will depend on the goals of the clinician or researcher. They will need to consider factors such as PROM domain (eg, quality of life, neuropathic pain), feasibility (eg, time, language accessibility, and licensing), and internal/external validity. Researchers should prioritize PROMs that are well validated and have established MICD to interpret the findings (eg, FACT/GOG-Ntx, EORTC-QLQ-CIPN20). 48 Patient-reported outcome measures with these characteristics are reported more often in the literature and can allow data to be combined and compared between studies and compiled into systematic reviews and meta-analyses. 48

Objective measures in CIPN are commonly used in clinical practice to identify or diagnose CIPN. As such, scoring of many of these measures is often threshold based, which favors a diagnostic as opposed to monitoring aim. Threshold-based scoring groups a final score into 2 categories (neuropathy or no neuropathy), which can easily identify if a patient has CIPN, but this does not allow the tracking of their progress over time in terms of symptom management or reduction. Objective measures can be used to assess many different domains of neuropathy. In addition to overall sensation, these measures can assess motor neuropathy symptoms, strength, reflexes, vibration sensitivity, sense of position, and electrical activity. In a recent review on CIPN measurements, the prevalence of sensory neuropathy and associated neuropathy symptom profiles (ie, motor, sensory, autonomic, etc.) differed between different chemotherapy types, showing the importance of measures to assess multiple different symptom domains of CIPN. 49 However, only 3 of the objective measures assess multiple different domains, and the Total Neuropathy Score (TNS) is the only measure that includes both sensory and motor symptoms of neuropathy. It is important to consider that while 6 of 8 objective measures have been validated, only 3 (TNS, Modified Inflammatory Neuropathy Cause and Treatment group sensory sumscore [INCAT-mISS], NCS) have been validated in a CIPN-specific population. The Total Neuropathy Score clinical (TNSc) version is the only measure with an established MCID for CIPN-specific populations.

Across all forms of neuropathy, NCS are defined as the gold standard and provide the reference for comparison to validate both PROMs and objective measures. 66 , 73 Nerve conduction studies provide additional mechanistic information on nerve function and electrical activity that other objective measures do not. 66 However, a recent review of clinical assessment strategies of CIPN including a Delphi survey among clinicians (which included oncologists and rehabilitation clinicians) and consumers, concluded that NCS were considered too burdensome for routine clinical use 66 due to their cumbersome nature, lengthy assessment time, and need for specialized training and equipment. In contrast, the TNS was most highly rated given it is easier to use yet still provides sensitive assessment of symptoms. 66 Importantly, the TNS still requires a lengthy assessment and needs in-depth training, so it is more burdensome to perform compared to more accessible measures such as cotton wool and 10 g monofilament testing. 49 As such, it is important to consider the amount of time, equipment, and training required to complete the assessments when selecting objective measures. Additional considerations when selecting objective measures include incorporating measures that assess a wider range of domains and symptom areas. This is important as CIPN symptoms can present differently across different treatment types. 49 This can be done using one comprehensive measure and/or using combinations of different measurement tools. Finally, when selecting measures to clinically assess neuropathy or to move research forward, it is important to use well-validated measures, preferably validated in a CIPN population, with reported MCIDs (eg, TNS, INCAT-mISS, NCS). Further research is needed to validate many objective measures in a CIPN-specific population and to fill the gap that many of these measures have in MCID reporting.

Limitations of our study include a lack of rigorous search strategy, which may not have detected all existing measurement tools meeting our inclusion criteria. However, our final compilation of measurement tools included more PROMs compared to a recent COSMIN review. 47 In addition, having only 2 authors involved in extracting measurement properties may limit the diversity of perspectives and increase the potential for selection and confirmation bias, potentially affecting the objectivity and comprehensiveness of the selection process. However, there was some checking of tools between authors, and results were reviewed by experts.

Conclusions

This review highlights the importance of selecting higher quality tools, such as ones with established MCIDs, and using a combination of objective and subjective tools to more comprehensively evaluate and understand a patient’s CIPN severity and functional impact.

The implementation of multiple assessment tools can provide a more comprehensive assessment or diagnostic approach of CIPN. The use of highly validated, gold standard measures on the objective side of measurement can provide an accurate assessment and diagnosis of CIPN, but also the accurate measurement of multiple domains associated with motor and sensory symptoms of CIPN. For this reason, measurement tools such as NCS and TNS may be useful. The use of highly validated PROMs such as the FACT/GOG-Ntx and EORTC-QLQ-CIPN20 can also add to the comprehensive assessment of CIPN, as it is important to understand the patient’s perspective on their symptoms and how their experiences compare to objective measurements. The objective measurement of multiple symptom domains and the subjective measurement through PROMs can allow for both the assessment of how CIPN symptoms may change over time, and the patient perception of those changes. However, when selecting measurement tools, it is also important to consider cost, training, and participant burden. In most trials, participants will need to complete measurements multiple times. Therefore, selecting assessment tools with a high ease of use and low burden to participants may increase acceptability.

In conclusion, the selection of CIPN measurement tools depends on the requirements of a study, as well as the goals of clinicians and researchers. To provide more well-rounded, high-quality results, validated and reliable tools should be used, capable of addressing many domains and symptom areas. As such, it may be wise to use a combination of PROMs and objective measurement tools to allow a better understanding of patients’ CIPN experience in order to guide clinical care and research.

Author contributions

Kaitlin Chen (Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Project administration, Validation, Writing—original draft, Writing—review & editing), Eric Antonen (Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Validation, Writing—original draft, Writing—review & editing), Michelle B. Nadler (Conceptualization, Methodology, Supervision, Validation, Writing—review & editing), Emma Mauti (Methodology, Validation, Writing—review & editing), and Jennifer M. Jones (Conceptualization, Methodology, Project administration, Resources, Supervision, Validation, Writing—review & editing)

Funding

No funding was provided to support this work.

Conflicts of interest

M.B.N. reports speaker honorarium and consulting fees from Novartis and Exact Sciences, outside of the scope of this submitted work. None other declared.

Data availability

No new data were generated or analyzed for narrative review.

Ethics approval and patient consent

No ethical review or patient consent was required for this review.

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