Pain in Platin-Induced Neuropathies: A Systematic Review and Meta-Analysis
Pain in Platin-Induced Neuropathies: A Systematic Review and Meta-Analysis
0 P. Zis (&) Academic Department of Neurosciences, Sheffield Teaching Hospitals NHS Foundation Trust , Sheffield , UK
1 A. Vadalouca Athens Medical Center , Athens , Greece
2 V. Brozou 251 Aviation General Hospital , Athens , Greece
Introduction: Platin-induced peripheral neuropathy (PIPN) is a common cause of PN in cancer patients. The aim of this paper is to systematically review the current literature regarding PIPN, with a particular focus on epidemiological and clinical characteristics of painful PIPN, and to discuss relevant management strategies. Methods: A systematic computer-based literature search was conducted on the PubMed database. Results: This search strategy resulted in the identification of 353 articles. After the eligibility assessment, 282 articles were excluded. An additional 24 papers were identified by scanning the reference lists. In total, 95 papers met the inclusion criteria and were used for this review. The prevalence of neuropathic symptoms due to acute toxicity of oxaliplatin was estimated at 84.6%, whereas PN established after chemotherapy with platins was estimated at 74.9%. Specifically regarding pain, the reported prevalence of pain due to acute toxicity of oxaliplatin was estimated at 55.6%, whereas the reported prevalence of chronic peripheral neuropathic pain in PIPN was estimated at 49.2%. Conclusion: Peripheral neuropathy is a common complication in patients receiving platins and can be particularly painful. There is significant heterogeneity among studies regarding the method for diagnosing peripheral neuropathy. Nerve conduction studies are the gold standard and should be performed in patients receiving platins and complaining of neuropathic symptoms post-treatment.
Cancer; Platin; Polyneuropathy
The term ‘‘peripheral neuropathy’’ (PN) refers to
various disorders of the peripheral nervous
system, including single and multiple
(asymmetric) mononeuropathies, symmetrical
involvement of many nerves (polyneuropathy),
or the sole involvement of the dorsal root
PN is very prevalent in cancer patients [
and can be a direct or an indirect complication
of cancer or cancer-related treatment, a
pre-existing comorbidity not related to cancer, or part
of a paraneoplastic syndrome [
The vast majority of chemotherapy-induced
PN (CIPN) is caused by neurotoxic
chemotherapy schemes, with platins (cisplatin,
oxaliplatin, carboplatin) constituting the leading
source of treatment-induced PN in cancer.
Contrary to the perception that painful
neuropathies are largely caused by diabetes, other
forms of PN can be particularly painful, leading
to poor quality of life [
platin-induced peripheral neuropathy (PIPN) should be
considered a major cause of pain in cancer
The aim of this paper is to systematically
review the epidemiological and clinical
characteristics of painful PIPN and provide an
overview of relevant management strategies.
Literature Search Strategy
A systematic computer-based literature search
was conducted August 15, 2017, on the PubMed
database. For the search, we used three Medical
Subject Headings (MeSH) terms in either the
title or abstract, as follows: (1) ‘‘neuronopathy’’
or ‘‘ganglionopathy’’ or ‘‘neuropathy’’ or
‘‘polyneuropathy’’; (2) ‘‘pain’’ or ‘‘painful’’; (3)
‘‘chemotherapy’’ or ‘‘platin’’ or ‘‘platins’’ or
‘‘oxaliplatin’’ or ‘‘cisplatin’’. Articles were limited to
English language, species to human, and with
full text available. We also perused the reference
lists of the papers in order to identify papers not
found through the search strategy.
Inclusion and Exclusion Criteria
Articles eligible for inclusion in the review were
required to meet the following criteria:
1. Involved case series with platin-induced PN.
2. Studied human adult subjects.
The following were excluded:
1. Book chapters, reviews, letters to the editor,
and editorials that did not provide new
2. Papers providing incomplete clinical or
neurophysiological data about the single
Data were extracted from each study in a
structured coding scheme using Microsoft
Excel, and included information on the article
identification, year of publication, evaluation
period, total number of subjects, gender, age,
presence of pain in general, presence of pain
secondary to the neuropathy,
neurophysiological type of neuropathy, course of symptoms,
type of cancer, and type of platin. We also
collected information about the time point of
diagnosis in each study, and whether they
referred to acute toxicity or cumulative effect
after completion of all cycles of chemotherapy.
Papers referring to symptoms during
chemotherapy without specifying the time
point (such as which cycle) were not considered
A database was developed using IBM SPSS
Statistics software (version 23.0 for Mac; IBM
Corp., Armonk, NY, USA). Frequencies and
descriptive statistics were examined for each
variable. The primary outcome of interest was
the proportion of patients who experienced
pain because of PIPN.
Compliance with Ethics Guidelines
This article is based on previously conducted
studies and does not involve any new studies of
human or animal subjects performed by any of
This search strategy resulted in the
identification of 353 articles. A total of 282 articles were
excluded during the eligibility assessment, and
25 additional papers were identified by
scanning the reference lists. Therefore, 96 papers
met the inclusion criteria and were used for this
]. These studies were published
between 1980 and 2017. Figure 1 illustrates the
study selection process.
Full clinical and neurophysiological data
were further extracted from 54 papers [
involving a total of 8159 patients (49.8% male)
who received chemotherapy that included
platins. The age of the patients ranged from 18 to
85 years (mean 65.9 years). The demographic
and clinical characteristics of these patients are
summarized in Table 1.
Forty-six papers provided data for the
prevalence of PN in patients who received
platins in their chemotherapeutic scheme. Of
these, 22 papers reported PN during
chemotherapy, 14 reported PN after completion
of chemotherapy, and three specifically
reported the acute toxic effects of oxaliplatin. Seven
papers did not clearly specify the time point
where PN occurred. The prevalence of
established PN after chemotherapy was estimated at
In 16 studies, patients received only platins,
not combined with another neurotoxic
chemotherapeutic agent. Of these, four papers
Number of patients per study, mean (SD) 151.1 (419.6)
Number of papers*
Total number of patients
Mean age, in years
Diagnosis of PN
Questionnaires only (%)
Nerve conduction studies (%)
Quantitative sensory testing (%)
Clinical examination (%)
Not reported (%)
Platin-induced PN (%)
Painful PIPN (%)
*Providing full clinical and neurophysiological data
SD standard deviation, PN peripheral neuropathy
reported PN during chemotherapy, eight
reported PN after completion of chemotherapy,
and three specifically reported the acute toxic
effects of oxaliplatin. One paper did not clearly
specify the time point at which PN occurred.
The prevalence of neuropathic symptoms due
to acute toxicity of oxaliplatin was estimated at
84.6%, whereas established PN after
chemotherapy with platins was estimated at
74.9%. Of note, in only two studies—which
provided data about the prevalence of PIPN—
was PN confirmed with a full
Specifically regarding pain, the reported
prevalence of pain due to acute toxicity of
oxaliplatin was estimated at 55.6%, whereas the
reported prevalence of chronic peripheral
neuropathic pain in PIPN was estimated at 49.2%.
Epidemiological Characteristics of PIPN
A meta-analysis of 31 studies providing data from
4179 patients established that the prevalence of
CIPN was 68.1% (95% CI 57.7–78.4%) when
measured in the first month after chemotherapy
completion, 60.0% (95% CI 36.4–81.6%) at
3 months, and 30.0% (95% CI 6.4–53.5%) at
6 months or more [
]. However, these figures refer
to a variety of chemotherapeutic agents.
Moreover, the diagnosis of the neuropathy was not
made via nerve conduction studies (NCS) in all
cases; in some studies, neuropathy was based only
on quantitative sensory testing (QST),
neurological examination, and/or questionnaires [
Among only those studies in which NCS or QST
was used for assessment of neuropathy, the
prevalence of CIPN was higher: 73.3% (95% CI
58.6–87.3) within 1 month of chemotherapy
cessation, 70.1% (95% CI 41.8–98.4) at 3 months,
and 39.9% (95% CI 3.9–76.0) at 6 months or
greater. A limitation of these figures, however, is
that abnormal results obtained by QST without
having performed NCS does not definitively
establish the presence of PN, and thus the
above-mentioned percentages reflect the
presence of neuropathic symptoms rather than CIPN.
Specifically concerning platins, the incidence of
neuropathic symptoms for cisplatin ranged from
49% to 100%, whereas carboplatin was reported to
be less neurotoxic, with neuropathic symptoms
observed in 13% to 42% of cases [
presence of acute oxaliplatin-induced neuropathic
symptoms has been reported in 85–95% of
patients, and these symptoms have been observed
in a chronic persistent form in approximately
16–21% of patients [
11, 12, 56
Risk Factors for PIPN
Several risk factors have been associated with the
development of painful PIPN. Wang et al. [
reported that female sex, patient’s level of
functioning (assessed by the Eastern Cooperative
Oncology Group performance status scale), body
mass index (BMI), and baseline opioid use
were associated with increased severity of
oxaliplatin-induced peripheral neuropathy [
Attal et al. [
] revealed a significant relationship
between the severity of acute signs and symptoms
of oxaliplatin neurotoxicity after three cycles of
chemotherapy and the occurrence and severity of
chronic residual neuropathic symptoms as
assessed by QST and the Neuropathic Pain Symptom
Inventory (NPSI) after 1 year.
Moreover, the duration of neuropathic
symptoms was observed to increase as the
cumulative dose of platin increased [
example, Leonard et al. found that after the first
cycle of chemotherapy, the median duration of
dysesthesia was only 5 days, whereas it was
21 days in patients who received 12 cycles of
chemotherapy. The median duration of
paresthesia after cycle 1 was 7 days, but after cycle 12
was 21 days or longer [
]. Similarly, in many
clinical trials sensory symptoms causing
functional impairment have been found in only
about 15% of patients after a cumulative dose of
780–850 mg/m2 but in 50% of patients at a
cumulative dose of 1170 mg/m2 [
Specifically concerning carboplatin,
Takemoto et al. [
] observed a greater visual
analogue scale (VAS) score when it was combined
with paclitaxel than with docetaxel;
additionally, as the number of chemotherapy cycles
increased, the carboplatin–paclitaxel-induced
neuropathic symptoms became more severe.
Concerning cisplatin, Bezjak et al. [
demonstrated that in lung cancer survivors,
sensory cisplatin-induced neuropathic
symptoms were a late effect of cisplatin, persisting for
at least 9 months after chemotherapy and
affecting quality of life. Similar symptoms have
been reported as a late effect of cisplatin in
long-term survivors of testicular cancer, and the
cumulative dose of cisplatin has been reported
to be a major risk factor for the development of
Not all studies reported screening for
pre-existing neuropathy prior to chemotherapy
with platins. Also, not all studies reported
having excluded patients with other common risk
factors for PN such as diabetes, excessive
alcohol intake, gluten sensitivity [
hereditary neuropathies. Therefore, such
comorbidities may have contributed to the
development of PN.
Predictors of PIPN
Cold allodynia and hyperalgesia of the hands
after three cycles of oxaliplatin treatment was
found to be predictive of severe chronic
]. Among a range of cold stimuli,
pain induced by a 20 C stimulus to the hand
had the highest predictive value with regard to
development of severe chronic neuropathy. The
severity of chronic neuropathy was also found
to correlate with the duration of cold-evoked
symptoms, the intensity of acute neuropathic
symptoms, and the intensity of cold-evoked
Management of platin induced peripheral
neuropathic pain includes pharmacological and
non-pharmacological approaches [
Venlafaxine, a serotonin and norepinephrine
reuptake inhibitor, was effective in the
management of acute neuropathic symptoms in a
small series of patients receiving oxaliplatin
]. Venlafaxine also showed promising
preliminary evidence of clinical effectiveness of
this combination against chronic neuropathic
symptoms in oxaliplatin-induced PN [
According to the EFFOX study, complete relief
of neuropathic symptoms induced by
oxaliplatin was achieved in 31.3% of patients, which
is a significantly higher percentage than the
5.3% achieved with placebo [
Duloxetine, another serotonin and
norepinephrine reuptake inhibitor, was also found
to be effective in oxaliplatin-induced painful
]. In an open-label study, Yang
et al. demonstrated that duloxetine could be
used effectively in low doses (i.e. 60 mg/day)
without impairment of renal or liver function—
and importantly, without interfering with
]. More recently, a large
placebo-controlled randomized clinical trial
showed that duloxetine was more effective than
placebo in reducing the average PIPN pain score
after a 5-week treatment period [
duloxetine has the largest volume of evidence
supporting its use in the treatment of painful
Nortriptyline, a tricyclic antidepressant,
failed to demonstrate effectiveness for treating
paresthesia or pain in cisplatin-induced
neuropathic symptoms [
Topiramate showed promising preliminary
evidence of clinical effectiveness of this
combination against chronic neuropathic symptoms in
oxaliplatin-induced PN [
Carbamazepine, on the other hand, does not
appear to be beneficial against acute
oxaliplatin-induced painful neurotoxicity [
Research findings regarding the effectiveness
of gabapentin for treating pain caused by PIPN
remain controversial. In a phase III randomized,
double-blind, placebo-controlled crossover trial,
Rao et al. concluded that gabapentin failed to
demonstrate any benefit [
], whereas an
open-label study by Tsavaris et al. found that
gabapentin monotherapy seemed to be well
tolerated and useful for the management of
chemotherapy-induced neuropathic pain [
However, both studies included patients with
PN secondary to other chemotherapeutic agents
in addition to platins. To date, no study has
explored the efficacy of gabapentin alone in
patients with PIPN.
Liu et al. [
] reported that tramadol in
combination with acetaminophen, administered
in patients with colorectal or gastric
adenocarcinoma, was effective in relieving
oxaliplatin-induced peripheral neuropathic pain
]. Interestingly, this study proposed that
the A118G polymorphism of the mu-opioid
receptor gene (OPRM1) was a possible
mechanism for the reduced response to the
combination of tramadol and acetaminophen [
suggesting that management should be always
be tailored to individual patient
In an open-label study, Filipczak-Bryniarska
et al. demonstrated that the high-dose
capsaicin patch was effective in treating pain
associated with oxaliplatin-induced
]. However, this finding should be
interpreted with caution, given the limitations of
the study design and small number of the
There is some evidence that acupuncture may
be beneficial for the treatment of PIPN. In a
small case series, Donald et al. [
] reported that
patients with oxaliplatin-induced painful
neuropathy improved after acupuncture. Wong
et al. [
] similarly described a small series of
patients with symptoms of pain due to
carboplatin-induced neuropathy who improved after
acupuncture. A prospective pilot study by Hsieh
et al. [
] showed that laser acupuncture
relieved both cold and mechanical allodynia
induced by oxaliplatin in gastrointestinal
cancer survivors. To date, however, no large
randomized controlled trial has been conducted to
confirm the effectiveness of acupuncture in
managing pain in PIPN. Therefore, the current
evidence is weak.
Cunningham et al. [
] reported a case of
almost complete resolution of the tingling,
numbness, and pain of cisplatin-induced
neuropathy with manual therapy (massage) in a
patient with stage III esophageal
adenocarcinoma. However, as this was based on a single
case, this finding should be interpreted with
Henke et al. [
] reported that strength and
endurance training in patients receiving
platinum-based chemotherapy for lung cancer was
effective in managing pain. The authors thus
suggested that lung cancer patients should
receive enhanced physical activity intervention
during palliative chemotherapy.
Diagnosing and Monitoring PIPN
Large Fiber Neuropathy
The gold standard for diagnosing a large fiber
neuropathy is NCS. Although centers have
many different means of neurophysiologically
determining the presence of PN, sensory
conduction studies of sural and radial nerves are
recommended for the diagnosis of mild,
predominantly sensory axonal neuropathy [
This should be complemented with at least one
motor study, commonly of the tibial nerve, to
confirm motor involvement [
]. In the
case of PIPN, however, the neuropathy is
sensory, affecting the dorsal root ganglia. In a
sensory ganglionopathy, asymmetrical sensory
nerve action potentials (SNAPs) or complete
absence of SNAPs should be expected [
Small Fiber Neuropathy
Patients often complain of disabling symptoms
such as a burning sensation in the soles or the
fingertips, which is a common manifestation of
small fiber neuropathy (SFN). Nerve conduction
studies assess only large fibers, and therefore,
SFN cannot be excluded if NCS are normal.
The gold standard for a diagnosis of SFN is
skin biopsy; however, this is an invasive
technique and is thus usually avoided. QST is
commonly used for assessment of SFN, but this is
subjective. Alternatively, nerve morphology can
be rapidly assessed using in vivo corneal
confocal microscopy. This technique has been used
for the detection of various types of
neuropathy, including small fiber neuropathy [
Ferdousi et al. [
] showed that corneal confocal
microscopy was effective in detecting small
fiber neuropathy by a marked reduction in
corneal nerve morphological parameters in
patients with upper gastrointestinal cancer and
oxaliplatin- or cisplatin-induced neuropathy.
Several questionnaires have been used for the
detection and assessment of PIPN. Particular
interest has been focused on the development
and validation of questionnaires regarding
quality of life in patients with CIPN.
The European Organisation for Research and
Treatment of Cancer Quality of Life
Questionnaire C30 (EORTC QLQ-C30), designed to assess
quality of life for cancer patients, is widely used
and consists of 30 items comprising five
functional scales (physical, role, emotional,
cognitive, and social), global health status, and nine
symptom scales and single items (fatigue,
nausea and vomiting, pain, dyspnea, insomnia,
appetite loss, constipation, diarrhea, and
financial difficulties. It is also supplemented
with specific modules for the different cancer
16, 17, 83, 84, 95
The EORTC QLQ-CIPN20 is a quality-of-life
questionnaire developed to elicit patient
experience of symptoms and functional limitations
related to CIPN. It contains 20 items assessing
sensory, motor, and autonomic symptoms
]. The CIPN20 can assess frequency and
severity of painful CIPN in a wide range of
oncology patient populations.
The L-BASIC [location-based assessment of
sensory symptoms in cancer] instrument uses
location-specific ratings of sensory symptoms in
the cancer population [
]. It is structured such
that patients provide a numeric score and an
adjectival description for any sensory
symptoms, including both pain and neuropathic
sensations, present in each of 10 predefined
body areas [
The Rasch-built Overall Disability Scale for
CIPN (CIPN-R-ODS) is a Rasch-built
disease-specific interval measure suitable for
detecting disability and levels of activity and
participation in patients with stable disease
She Functional Assessment of Cancer
Group-Neurotoxicity (FACT/GOG-Ntx) questionnaire is the
Functional Assessment of Cancer
Therapy-General (FACT-G) instrument plus an
11-item subscale (Ntx subscale) [
]. It is a
chemotherapy treatment effect-specific
measurement tool used to evaluate the severity and
impact of CIPN symptoms on functional status
and health-related quality of life [
on the Ntx subscale include the feeling of
generalized weakness, numbness or tingling in the
hands or feet, and difficulty with fine motor
The Total Neuropathy Score (TNS) was
initially designed to evaluate diabetic neuropathy
] and was later validated in patients with
]. The TNS includes objective
measures, such as pin prick, vibration threshold,
and nerve conduction studies, combined with
subjective report of sensory, motor, and
autonomic items, and the instrument has been
tested in a variety of tumor types [
neuropathy-specific Neuropathic Pain Scale (NPS-CIN) is
a six-item scale used to assess CIPN and related
neuropathic pain severity [
25, 92, 93
The Patient Neurotoxicity Questionnaire,
comprising two items, defines the incidence
and severity of sensory and motor disturbances
The Chemotherapy-Induced Peripheral
Neuropathy Assessment Tool (CIPNAT)
contains 36 items that evaluate the occurrence,
severity, distress, and frequency of nine
neuropathic symptoms, along with 14 items that
evaluate neuropathic interference with
This systematic review has identified the
following key points:
1. PN is a common complication in patients
receiving platins in their chemotherapeutic
2. PIPN can be particularly painful. Acute
toxicity occurs only with oxaliplatin.
However, in a significant proportion of patients
receiving platins, the pain persists and
3. There is significant heterogeneity in the
methods used to diagnose PN. In many
studies, patients were diagnosed based only
on questionnaires or clinical examination.
Although the use of questionnaires may be
adequate for characterizing and monitoring
neuropathic symptoms, the gold standard
for accurate diagnosis of an established
peripheral neuropathy—from a
neurological point of view—is NCS. Ideally, this
should be performed as a baseline, before
the chemotherapy, and should be repeated
at the end or when symptoms occur. QST
alone is not sufficient for establishing a
diagnosis of PN, as it is not objective, and its
role is more as an indicator of small fiber
involvement; therefore, QST should be
complemented with NCS.
4. Small fiber neuropathy is gaining increasing
attention in clinical practice; however,
further studies are needed in patients receiving
platins, as the neuropathic pain that
patients experience during chemotherapy
with platins is likely often secondary to
small fiber involvement, with no
involvement of the large fibers.
Funding. No funding or sponsorship was
received for this study or publication of this
Authorship. All named authors meet the
International Committee of Medical Journal
Editors (ICMJE) criteria for authorship of this
manuscript, take responsibility for the integrity
of the work as a whole, and have given final
approval for the version to be published.
Disclosures. Vasiliki Brozou, Athina
Vadalouca, and Panagiotis Zis have nothing to
Compliance with Ethics Guidelines. This
article is based on previously conducted studies
and does not involve any new studies of human
or animal subjects performed by any of the
Data Availability. The data sets generated
and/or analyzed during the current study are
available from the corresponding author on
Open Access. This article is distributed
under the terms of the Creative Commons
Attribution-NonCommercial 4.0 International
by-nc/4.0/), which permits any noncommercial
use, distribution, and reproduction in any
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to the original author(s) and the source, provide
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indicate if changes were made.
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