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Facial Muscle Movements Encoding Pain: A Systematic Review

Abstract

Facial expressions of pain are not undefined grimaces, but they convey specific information about the internal state of the individual in pain. With this systematic review, we aim to answer the question of which facial movements are displayed most consistently during pain. We searched for studies that used the Facial Action Coding System to analyze facial activity during pain in adults, and that report on distinct facial responses (action units [AUs]). Twenty-seven studies using experimental pain and 10 clinical pain studies were included.

We synthesized the data by taking into consideration:

1. The criteria used to define whether an AU is pain-related
2. Types of pain
3. The cognitive status of the individuals

When AUs were selected as being pain-related based on a "pain > baseline" increase, a consistent subset of pain-related AUs emerged across studies: lowering the brows (AU4), cheek raise/lid tightening (AUs6_7), nose wrinkling/raising the upper lip (AUs9_10), and opening of the mouth (AUs25_26_27). This subset was found independently of the cognitive status of the individuals and was stable across clinical and experimental pain with only one variation, namely that eye closure (AU43) occurred more frequently during clinical pain.

This subset of pain-related facial responses seems to encode the essential information about pain available in the face. However, given that these pain-related AUs are most often not displayed all at once, but are differently combined, health care professionals should use a more individualized approach, determining which pain-related facial responses an individual combines and aggregates to express pain, instead of erroneously searching for a uniform expression of pain.

Introduction

The facial expression of pain has attracted considerable interest in experimental and clinical research based on an increasing awareness that it supports the communication of pain as a second signal system besides the verbal one, and thus can be used as another indicator of pain when self-report is missing (e.g., in patients with dementia). Right from the start of research on facial expressions of pain, researchers tried to characterize how facial activity during the experience of pain looks like. The vision was to define a prototypical facial expression of pain, similarly to prototypical facial expressions having been suggested for different emotional states.

Groundbreaking research was conducted by Prkachin, who analyzed in a sample of 41 healthy students which facial responses are displayed consistently across different types of experimental pain stimulation (pressure, temperature, electrical current, and ischemia). Facial responses were analyzed using the Facial Action Coding System (FACS), the gold standard for facial expression research. The FACS is a fine-grained, objective, and anatomically based coding system that differentiates between 44 facial movements (action units [AUs]). Coders are trained to apply specific operational criteria to determine the onset and offset as well as the intensity of the AUs.

Using the FACS, Prkachin suggested that there are four facial movements that are more steadily displayed across experimental pain modalities than other AUs:

• Lowering the brows (AU4)
• Cheek raise/lid tightening (AUs6_7)
• Nose wrinkling/raising the upper lip (AUs9_10)
• Eye closure longer than 0.5 seconds (AU43)

Prkachin and Salomon further suggested that this set of facial movements is not only indicative for experimental pain but also for clinical pain. When studying facial responses in a group of 129 shoulder pain patients undergoing a range of painful movement exercises, the authors found that the same set of facial movements was displayed as had been previously found for experimental pain. Mainly based on these two studies, this subset is regarded as presenting the key components of the facial expression of pain.

Meanwhile, a substantial number of further studies have been conducted, investigating facial expressions of pain in various groups of individuals (e.g., young, old, patients with depression, individuals with intellectual disabilities) and during various types of pain conditions (low back pain, chest pain, and experimental pain). At least parts of the above-described set of facial responses have also been found to be associated with pain in these further studies. Nevertheless, there is also considerable variability between studies, with other facial movements also having been found to be pain-related. For example, "raising the chin" (AU17) or even "oblique lip raising" (AU12, smiling) have been recurrently found to occur while individuals are experiencing pain. Indeed, some studies include up to 17 AUs as a set of pain-associated AUs.

One reason for the variability between studies is the difference in how studies defined whether an AU is pain-related. Overall, there are two main approaches:

1. Frequency of Occurrence Criterion: An AU is defined as pain-related when it occurs during pain above a critical frequency level, which is often set to 5%.
2. Pain > Baseline Criterion: An AU is defined as pain-related when it occurs statistically more frequently during pain compared with a non-painful baseline condition, or more frequently in pain patients compared with pain-free controls.

Often, approach two is not conducted on all possible 44 AUs of the FACS system. Instead, authors use approach two consecutively after having used approach one to preselect AUs that fulfil the frequency of occurrence criterion, and then in a second step, the pain > baseline criterion is used to define which of these preselected AUs are really pain-related.

The aim of this systematic review is to examine the question of which facial movements are indeed pain-related by making use of the substantial number of primary studies that have analyzed facial responses during pain. We take into consideration:

1. The different criteria used to define whether an AU is pain-related
2. Different types of pain (clinical vs experimental pain)
3. The cognitive status of the individuals being examined

Given that FACS is the most often used and best operationalized method to analyze facial expressions of pain, we limited our review to those studies using FACS, although other methods can also be used to assess facial communication of pain (e.g., non-FACS-based automatic systems and observational pain scales).

Methods

The systematic review was performed following the Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols.

Search Strategy and Study Selection

Literature Search

An extensive search of literature published until April 2018 was conducted using the databases PubMed and PsycINFO. No restrictions were set with regard to the earliest year of publication. The search combined keywords for pain (pain, nociception) with keywords for facial expression (facial expression, facial display, facial activity, facial expressiveness, facial response, FACS) using logical AND and OR operators.

Given that we were interested in facial activity during pain in human adults, the following keywords were excluded using a NOT qualifier:

• Child
• Neonat*
• Animal

In addition, reference lists from identified articles as well as reviews and book chapters on facial expression of pain were screened for missing articles. The systematic search was limited to articles published in English or German.

Eligibility Criteria

Studies were selected based on the following inclusion criteria:

1. Facial responses were analyzed using the FACS
2. Results were provided on single AUs
3. A minimum sample size of N = 20 was included
4. A clear description of statistics was provided

Non-original research, conference proceedings, and doctoral theses were excluded. Two independent reviewers screened the titles and abstracts for the eligibility criteria. Full texts of all potentially relevant studies were retrieved. In cases of discrepancies or disagreement between the two reviewers, a third reviewer was consulted and discrepancies were resolved.

Information Extraction

From each included study, the following information was extracted:

1. Sample: Patients or healthy participants, number of participants, age, sex, and cognitive status
2. Type of Pain: Experimental pain (pressure, thermal, electrical, or other procedures such as blood sampling or injections) and clinical pain
3. FACS Coding: Duration of sampling, how many and which AUs were coded, and AU information being coded (intensity, frequency, duration, and apex)
4. Approach Used to Determine Pain-Related AUs: Selection based on a frequency of occurrence criterion or a pain > baseline criterion

Information was extracted by one reviewer and independently verified by a second reviewer. To control for bias caused by the inclusion of multiple reports of the same study, authors were contacted in cases where an overlap of the sample was suspected and duplicate samples were excluded. All ambiguities in data extraction (6% reviewer discrepancies) were double-checked and resolved.

Assessing the Quality of Studies

To assess the quality of the studies and the risk of bias, studies were graded according to pre-specified quality criteria.

Source: FaceReader pain encoding, Noldus Information Technology