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Keywords: Lionfish, Pain, Envenomation, Sting, Questionnaire
Abstract
Introduction:
Stings from the lionfish (Pterois volitans) constitute one of the most painful wounds in the ocean. This species has invaded the Atlantic coast of the United States, Gulf of Mexico, Caribbean, and Mediterranean Sea. In addition to its ecological impact on local fish populations, stings from the lionfish pose a medical problem because of the debilitating nature of the pain they produce. However, there are no studies examining the human pain experience of lionfish stings.
Objective:
To characterize the various aspects of the pain experience following a lionfish sting.
Methods:
We developed a pain questionnaire that includes validated scales used with patients having acute or chronic pain to understand the pain variability, as well as the use of health care resources and treatments.
Results:
We provide the first study of the pain experience from lionfish stings. Here, we show that the pain is intense from the start and peaks approximately 1 hour later, resolving itself in 7 days for most victims. Furthermore, pain intensity can be influenced by several factors, including (1) age of the victim, where older victims experience significantly higher pain intensities, (2) the number of spines involved, (3) and whether infection occurred at the injury site. However, pain intensity was not different between male and female participants.
Conclusion:
These findings will inform the medical community on the pain experience and can be used by local authorities to better appreciate the impact of lionfish envenomations to develop programs aimed at curtailing the expansion of the lionfish.
1. Introduction
The lionfish (Pterois volitans) is a venomous fish endemic to the Indo-Pacific that has, over the past 30 years, invaded the Caribbean, Gulf of Mexico, Northwestern Atlantic, and Mediterranean Sea. The fish has spread at an alarming rate because of its rapid reproductive capacity and its lack of natural predators in the invaded regions.23 Lionfish tend to predate any fish smaller than them, resulting in a steep reduction in reef biodiversity in affected areas.6,13,17,22,23,26 These effects on the ecosystem have led local governments to setup spearfishing initiatives to control the spread of the lionfish. This resulted in a rapid increase in the number of individuals handling lionfish and ultimately in the number of stings.20 Although initiatives aimed at curtailing this invasion focus on limiting ecological impact, the medical aspect of this invasion must also be appreciated. This includes the pain that is experienced by victims of lionfish stings, which can affect various aspects of daily life.
Lionfish stings occur when a victim's skin is punctured by one or more of their 18 venomous spines. These cartilaginous spines are coated with an integumentary sheath, underneath which is the venom gland tissue. Once skin is punctured by a spine, the sheath is torn, and venom diffuses into the victim.15,20,27 Lionfish stings produce painful sensations and result in swelling, redness, and many other unpleasant symptoms.1,12,14,19,20,24 However, there is no data regarding the venom's toxin composition, and little understanding of the venom's molecular mechanism of action. A prior preclinical study from our group characterized the pain following intraplantar injections of lionfish venom in mice, as well as a cellular characterization of the venom's activity on nociceptors.16 Although that study helped understand pain following lionfish sting, the pain experienced by humans following lionfish stings remains poorly documented and understood. There exist numerous case studies of extreme envenomations,1,12,14,19,20,24 but because the average lionfish sting does not usually result in hospitalization, there are no characterizations of the average human pain. In addition, case studies mostly place a focus on the swelling, redness, and nonpain symptoms of lionfish envenomations. Yet, pain is the cardinal symptom reported from lionfish stings.
There is an overall lack of pain-focused questionnaires for victims of stings from any species, and those that have been done did not take advantage of well-validated scales, thus lacking standardization and making results hard to compare.28 We sought to solve this problem by assembling a pain questionnaire designed for victims of lionfish sting, including validated scales/questionnaires used with patients having acute or chronic pain from a variety of different underlying sources. The objectives of this study were (1) to characterize various aspects of the pain experience by victims of lionfish sting, including its severity, qualities, and impact on various aspects of daily life, (2) to investigate contributions of various factors in the variability of pain experience including factors surrounding the sting itself, and (3) document the use of health care resources and treatments used to control the pain associated with lionfish sting.
2. Methods
2.1. Study design and setting
We assembled a questionnaire to investigate the pain caused by lionfish envenomations and to quantify and analyze factors surrounding the envenomations that may or may not affect pain and discomfort. This questionnaire was composed of 44 questions and hosted at the URL www.lionfishpain.org. The questionnaire was created using the survey platform Typeform and integrated into the hosting URL. To prevent duplicate submissions, responders were asked whether they had completed the questionnaire before, and if they responded “Yes,” their second submission was not considered in our analysis. Furthermore, duplicate email addresses, which were voluntarily submitted by most participants, were flagged, and second submissions from these individuals were not considered in our analysis.
The protocol was approved by the Faculty of Medicine and Health Sciences Institutional Review Board of the McGill University on February 3, 2021 (A02-M09-21B), and it was conducted in conformity with the published guidelines of the Tri-Council Policy Statement 2, in compliance with the Plan d'action ministériel en éthique de la recherche et en intégrité scientifique (MSSS, 1998), and the Food and Drugs Act (17 June 2001); it acts in accordance with the US Code of Federal Regulations that govern research on human subjects (FWA 00004545). Participants were automatically assigned a token ID number by Typeform, and once data were exported, nominal data and token ID numbers were separated from the main file and kept in a separate password-protected Excel file. From that point onward, only the token ID numbers were associated with participant data, and all nominal data were removed from the main analysis file.
2.2. Participant recruitment
The questionnaire was advertised by email and distributed through a variety of marine biologists who study the lionfish, as well as on social media accounts through lionfish hunters and within their communities. The questionnaire was also advertised at a variety of lionfish hunting events across Florida. Cards with the website URL and information on the questionnaire were distributed at a variety of lionfish hunting events and through lionfish hunting communities to people who were interested.
2.3. Procedures
Using targeted questions, adapted from the standardized NIH PROMIS questionnaire (for pain intensity),8,11 the short-form DN4 questionnaire (for pain characteristics),4,18 and some context-specific questions, we sought to gain insights into the characteristics of the sting sites, intensity of the victims' pain, and the qualities of their pain. Furthermore, we assessed the interference of the pain on daily activities using the Brief Pain Inventory. Overall, respondents were asked to quantify pain intensity over 5 different time points, qualities of their pain, how pain interfered in their normal lives, and a variety of different factors that we hypothesized may affect the pain caused by a lionfish sting. The questionnaire was made public online on February 23, 2021, and was available up to February 2022. We received 605 submissions within 1 year (analyses for this study were performed using data collected up until February 2022). Exclusion criteria for responses included long delays between the sting event and completing the questionnaire (more than 10 years), incomplete filling of the questionnaire (more than one-thirds of the questionnaire left unanswered), third-party reports of lionfish stings, and duplicate reports of lionfish stings from the same individual. Our host URL, lionfishpain.org received 901 unique visitors between February 23, 2021, and February 25, 2022, 652 of these individuals were located in the United States, 65 in Canada, 35 in the United Kingdom, 32 in Bonaire, and the rest were spread across the world (48 other countries).
Using the short-form DN4 questionnaire, we asked participants to report whether their pain matched any of the following qualities to gain insights into whether the pain caused by a lionfish sting had any neuropathic qualities. For each participant, a “yes” to each of these qualities was scored as a value of 1, and their DN4 score was tabulated based on counting how many of these qualities each patient reported, for which the maximum score was 7.
We asked participants to complete a series of pain interference questions using a modified version of the Brief Pain Inventory (BPI) Pain Interference Scales 109,11 and indicate a score from 0 to 10 for how much each of the named activities were affected due to the pain they experienced following a lionfish sting. Items that were considered for this score included general activity, mood, walking ability, normal work, sleep, enjoyment of life, and social activities. A global pain interference score was calculated for each patient by calculating the sum of their scores in each category, with a maximum possible score of 70.
To characterize the time course of the pain experienced by sting victims, we asked participants to score the intensity of their pain on the NIH PROMIS Short Form Pain Intensity Questionnaire on a scale of 0 to 10, where 0 indicated no pain, and 10 worst imaginable pain at 5 different time points: immediately after the sting, then 1, 2, 3, 24 hours, and 1 week after the sting.
2.4. Statistical analysis
Data were exported from Typeform and saved as a .csv file to reformat the data for analysis. All analyses were performed using Python. Descriptive statistics were used to depict the participants' demographics, the characteristics of their pain experience, and the types of pain management modalities they used. Mean, median, standard deviation, and interquartile range (IQR) values were computed for continuous variables, whereas percentages and frequencies were computed for categorical variables. The evolution of pain over time was analyzed using a mixed model for repeated measurements (MMRM), considering participants' sex and age, history of allergies, fish status (live or dead), number of spines involved in the sting, and whether the sting ultimately resulted in an infection. The type of variance–covariance matrix was compound symmetry. An analysis of covariance (ANCOVA) was performed to identify factors statistically associated with pain at each time of measurement. Mixed model for repeated measurements and ANCOVA analyses were performed using SAS software (version 9.4; SAS Institute Inc, Cary, NC).
3. Results
3.1. Characteristics of the responders
In the 1-year period during which we collected responses to our survey, we received 605 submissions, 50 of which we had to remove because of a variety of exclusion factors (see Methods). Table 1 and Figure 1 show the demographic characteristics of the responders (N = 555). Close to 80% were males with a mean age of 46.71 years (SD = 13.23) (Table 1 and Fig. 1A, B). The median time elapsed between the sting and the completion of the questionnaire was 336 days (interquartile range, 580 days).
Table 1.
Demographic data describing lionfish pain questionnaire participants.
Age, y | |
Under 20 | 7 |
20–29 | 52 |
30–39 | 127 |
40–49 | 116 |
50–59 | 157 |
60–69 | 71 |
70–79 | 24 |
Mean (SEM) | 46.71 (0.5622) |
Sex | |
Male | 441 |
Female | 109 |
Race | |
White | 509 |
Hispanic or Latino | 26 |
Black or African American | 4 |
Asian/Pacific Islander | 4 |
Other | 11 |
Time since sting | |
Mean (SEM) | 1854.479 (298.47) |
Median | 336 |
Mode | 730 |
Survey responses regarding responders' age, sex, and race as well as the delay in days between the sting and responding to the questionnaire. Data are expressed as counts (N) with percentage distributions indicated in brackets or means with standard deviations in brackets (SD), as indicated.
Figure 1.
Description of sting survey participants' sex, age and activity they were doing at the time of their lionfish sting. (A) Pie chart depicting distribution of male vs female participants. Number following comma indicates the number of participants. (B) Pie chart depicting age distribution of participants. Number following comma indicates the number of participants. (C) Bar chart demonstrating different activities performed by participants at the time of their lionfish sting.
3.2. Circumstances surrounding the lionfish stings
As shown in Table 2, the most common activities performed by participants at the time of their lionfish sting were spearfishing (72.07% of participants, Fig. 1C blue bar and Table 2) and diving or snorkeling (14.95% of participants, Fig. 1C purple bar and Table 2). Furthermore, the most stung body part was the hand/arm (90.63% of participants, see Table 2), consistent with common lionfish sting injuries stemming from spearfishing and diving/snorkeling. Most of the questionnaire participants were in the United States at the time of their sting (67.03% of participants, see Table 2), with the majority of the others distributed across the Caribbean, consistent with the fact that lionfish are invasive in the Gulf of Mexico and Caribbean.
Table 2.
General data describing context of reported lionfish stings.
Body part | |
Hand/arm | 503 |
Foot/leg | 46 |
Torso | 4 |
Face/head | 2 |
No. of spines | |
1 spine | 340 |
2 spines | 128 |
3+ spines | 81 |
I don't remember | 5 |
Activity at the time of the sting | |
Spearfishing | 400 |
Cleaning/fileting a lionfish | 45 |
Cleaning my tank | 7 |
Diving/snorkeling | 83 |
Other | 20 |
Country | |
United States | 372 |
Bonaire | 32 |
Honduras | 29 |
Belize | 18 |
Bahamas | 16 |
Aruba | 11 |
Cayman Islands | 7 |
Curacao | 7 |
US Virgin Islands | 6 |
Mexico | 6 |
Nicaragua | 5 |
Dominica | 5 |
Other | 41 |
Stung by a live fish | 477 |
Stung underwater | 481 |
History of allergies | 123 |
Stung area got infected | 18 |
Survey responses regarding context of lionfish stings, including the body part stung, the number of spines involved in the sting, the activity the individual was performing at the time of the sting, and the country the sting took place in. Bottom 4 rows represent further details providing context to the sting including whether the sting took place underwater and by a live lionfish, whether the victim has a history of allergies, and whether the stung area ultimately got infected during their recovery from the lionfish sting. Data are expressed as counts with percentage distributions indicated in brackets.
For the 85.95% of participants, the lionfish was alive at the time of their sting (Table 2), and for 86.67% of participants, the sting took place underwater (Table 2). Finally, we found that 22.16% of participants had a history of allergies, and only 3.24% of participants experienced an infection at the site of their sting in the days and weeks following the sting (Table 2).
3.3. Sting characteristics and pain qualities
As shown in Table 3, all participants experienced pain after the sting. Three-quarters of the responders (76.22%) reported that their pain was continuous, whereas it was an intermittent type of pain in the other cases. Other sting characteristics included reported soreness (69.37% of the participants), redness (68.83% of the participants), swelling (85.59%), bruising (11.71%), blistering (11.53%), paleness (7.75%), and necrosis (4.68%).
Table 3.
Data describing details of sting appearance, pain intensity, and pain qualities.
Characteristics of stung area, N (%) | |
Redness | 382 (68.83%) |
Paleness | 43 (7.75%) |
Swelling | 475 (85.59%) |
Bruising | 65 (11.71%) |
Blistering | 64 (11.53%) |
Necrosis | 26 (4.68%) |
Pain intensity (score/10), mean (SD) | |
Immediately after the sting | 4.973 (2.40) |
1 h after the sting | 7.252 (2.69) |
2 h after the sting | 6.10 (3.01) |
1 d after the sting | 2.87 (2.49) |
1 wk after the sting | 1.05 (8.99) |
Pain qualities, N (%) | |
Soreness | 385 (69.27%) |
Burning | 309 (55.68%) |
Cold | 24 (4.32%) |
Electric shocks | 54 (9.37%) |
Tingling | 258 (46.49%) |
Pins and needles | 198 (35.68%) |
Itchiness | 211 (38.02%) |
Numbness | 255 (45.95%) |
DN4 score (mean (SD)) | 2.359 (1.61) |
Continuous or intermittent pain, N (%) | |
Continuous | 423 (76.22%) |
Intermittent | 132 (23.78%) |
Other symptoms, N (%) | |
Nausea | 80 (14.41%) |
Sweating | 93 (16.76%) |
Trouble sleeping | 54 (9.73%) |
Accelerated heart rate | 74 (13.33%) |
Shock | 18 (3.24%) |
Fainting | 10 (1.80%) |
Top: Participants self-reported visual features of their sting. Data are expressed as counts with percentage distributions indicated in brackets. Second: Participants self-reported pain intensity information in an adapted PROMIS questionnaire format. They were required to report pain from 1 to 10 at the different timepoints. Data are presented as mean (SEM). Third: Participants self-reported different qualities of their lionfish sting–induced pain based on the DN4 questionnaire, to tabulate a DN4 score. They also indicated whether their pain was continuous or intermittent. Bottom: Participants self-reported any other symptoms that have previously been reported with lionfish stings.
Table 3 shows the results obtained on each item of the DN4 Questionnaire. The most common reported sensations were burning sensation (55.68%), tingling (46.49%), and numbness (45.95%) (Table 3). The mean DN4 score was 2.36 (±1.61) out of a maximum possible score of 7 (Table 3).
Less common symptoms experienced (and their abundances) were nausea (80 of 555 or 14.41% of participants), sweating (93 of 555 or 16.76%), trouble sleeping (54 of 555 or 9.73%), accelerated heart rate (74 of 555 or 13.33%), shock (18 of 555 or 3.24%), and fainting (10 of 555 or 1.80%) (Table 3).
3.4. Pain intensity
The mean (±SD) pain rating immediately after the sting was 4.97 (±2.40) and peaked to 7.25 (±2.69) at 1 hour after the sting (Table 3). This number dropped to 6.10 (±3.01) at 2 hours after the sting, and it was still present the following day at 2.87 (±2.49). It eventually dissipated a week later, reaching 1.05 (±8.99).
3.5. Pain interference on daily living
We sought to evaluate how the pain experience from a lionfish sting can affect an individual's normal activities. Table 4 shows the extent to which lionfish sting pain affected various aspects of daily living. In the BPI Pain Interference scales, scores at or above 4 out of 10 indicate moderate to severe interference. In our study, most scores were lower than 4 out of 10, with the highest scores being general activity (3.63 ± 2.49) and normal work (3.52 ± 3.09). Other categories for which responders reported low interference included self-care (2.18 ± 2.93), recreational activities (2.97 ± 2.95), mood (2.60 ± 2.33), walking ability (0.96 ± 2.31), sleep (2.55 ± 2.96), enjoyment of life (2.25 ± 2.91), and social activities (1.89 ± 2.99) (Table 4). More than two-thirds of the participants (69.37%) reported having needed to take time off from work because of their lionfish sting, reporting on average 17.98 (±17.33) hours of work missed.
Table 4.
Self-reported life interference details (score on 10) caused by pain and discomfort caused by lionfish stings as well as participants' time lost from work (if needed) because of lionfish sting.
Altered activities (score/10) mean (SD) | |
Self-care | 2.184 (2.93) |
Recreational activities | 2.971 (2.95) |
General activity | 3.631 (2.49) |
Mood | 2.602 (2.33) |
Walking ability | 0.962 (2.31) |
Normal work | 3.515 (3.09) |
Sleep | 2.550 (2.96) |
Enjoyment of life | 2.245 (2.91) |
Social activities | 1.897 (2.99) |
Pain interference score | 17.402 (15.91) |
Missed work (N (%)) | 385 (69.37%) |
Data are reported as mean (±SD) of the reported score on 10.
3.6. History of stings
As shown in Table 5, just less than half of the participants (41.98%) had prior experiences with lionfish stings. The characteristics of the stings were similar to the one depicted for the most recent one. Almost half of the responders (47.64%) who had been stung before indicated that the pain was less intense than previous stings, whereas 39.48% (92 of 233 participants) reported that the pain was the same (Table 5). Only 13.3% indicated that their pain was more intense than that from past lionfish stings.
Table 5.
Details of past stings reported by participants who had been stung by lionfish before the sting reported in first part of questionnaire.
Stung in the past (N (%)) | 233 (41.98%) |
Stung body part, N (%) | |
Hand/arm | 213 (91.42%) |
Foot/leg | 17 (7.30%) |
Face/head | 1 (0.43%) |
Activity when sting occurred, N (%) | |
Spearfishing | 180 (77.28%) |
Fileting a lionfish | 18 (7.73%) |
Diving/snorkeling | 24 (10.30%) |
Other | 11 (4.72%) |
No. of spines involved, N (%) | |
1 spine | 174 (74.67%) |
2 spines | 23 (9.87%) |
3+ spines | 25 (10.73%) |
Pain compared with previous sting, N (%) | |
The same | 92 (39.48%) |
Less intense | 111 (47.64%) |
More intense | 31 (13.30%) |
Data are reported as counts with percentage distributions indicated in brackets.
3.7. Factors associated with pain intensity
Figure 2 and Table 6, respectively, show the results of the MMRM analysis and the ANCOVAs using the general linear model procedure used to identify factors influencing variability in pain intensity following lionfish stings. We observed no significant sex differences in pain from lionfish stings (see Fig. 2A, Table 6 and supplemental Table 1, available at http://links.lww.com/PR9/A202). The fact that the lionfish was alive or dead at the time of the sting did have a significant effect on pain at specific time points. Although we did not find that the fish being alive or dead had a global impact on reported pain in the MMRM analysis (although the result was close to statistical significance with P = 0.0595), the results of the ANCOVAs revealed that the variable had a significant influence on pain at specific time points. Immediately after the sting, there was no significant difference in pain between dead or alive fish groups, but there was a significant difference at 1 and 2 hours after the sting (P = 0.0304 and 0.0193, respectively, ANCOVA, Fig. 2B, Table 6 and supplemental Table 1, available at http://links.lww.com/PR9/A202). Age was a variable that caused significant variation in pain experienced by sting victims, playing the largest role at 1 and 2 hours after the sting (1 hour later: P = 0.0002 and 2 hours later: P = 0.0298, repeated ANCOVAs with general linear model procedure, see Table 6 and Supplemental Table 1, available at http://links.lww.com/PR9/A202). On average, older participants reported more intense pain than younger ones with the 50 to 59-year-old, 60 to 69-year-old and 70 to 79-year-old groups reporting more pain overall than the younger than 30 years group (P = 0.0175, 0.0019 and 0.0038, respectively, in the MMRM analysis, see Supplemental Table 1, available at http://links.lww.com/PR9/A202 and Fig. 2C). The sting victims' history of allergies had no effect on pain at any time point (see Fig. 2D, Table 6 and Supplemental Table 1, available at http://links.lww.com/PR9/A202).
Figure 2.
Self-reported lionfish pain over the course of 1 week after a sting. Mean (±SD) self-reported pain on 10 immediately after a lionfish sting, 1 hour later, 2 hours later, 1 day later, and 1 week later. (A) Male (441 individuals) vs female (109 individuals) participants. (B) Participants' pain divided based on whether the fish that stung them was alive (477 individuals) or dead (78 individuals). (C) Participants divided based on age range (younger than 30 years: 60 individuals, 30-39 years: 127 individuals, 40-49 years: 116 individuals, 50-59 years: 157 individuals, 60-69 years: 71 individuals, 70-79 years: 24 individuals). All statistical comparisons are relative to younger than 30 years age group, *P < 0.05, **P < 0.01. (D) Participants who have allergies (123 individuals) vs do not have allergies (432 individuals). (E) Participants' pain divided based on how many spines punctured the skin during the sting event (1 spine: 340 individuals, 2 spines: 128 individuals, 3+ spines: 81 individuals, unknown number of spines [not shown]: 5 individuals). ***P < 0.001 (1 spine vs 3 spines). (F) Participants' pain divided based on whether their sting ultimately got infected (infected: 18 individuals, not infected: 537 individuals), *P < 0.05. Mixed model for repeated measures analysis for all panels.
Table 6.
Statistical analysis of variables influencing pain experienced by the victim of sting at different time points.
Time point | Variable | F | P | Time point | Variable | F | P |
---|---|---|---|---|---|---|---|
Pain immediately | Age Sex Allergies Infection Delay since sting Number of spines Fish alive 1st time stung Time off work |
1.76 0.01 0 0.44 3.23 0.22 1.23 2.63 0.26 |
0.119 0.911 0.962 0.508 0.022 0.805 0.267 0.106 0.613 |
Pain next day | Age Sex Allergies Infection Delay since sting Number of spines Fish alive 1st time stung Time off work |
0.6 0.01 0.97 7.34 0.62 10.74 1.58 4.41 0.49 |
0.699 0.933 0.324 0.007 0.605 <0.0001 0.209 0.036 0.483 |
Pain 1 h later | Age Sex Allergies Infection Delay since sting Number of spines Fish alive 1st time stung Time off work |
5.03 0.01 0.26 4.54 12.39 5.36 4.71 2.7 0.01 |
0.0002 0.923 0.609 0.034 <0.0001 0.005 0.0304 0.101 0.934 |
Pain next week | Age Sex Allergies Infection Delay since sting Number of spines Fish alive 1st time stung Time off work |
0.6 1.54 0.35 8.36 0.11 5.8 0.52 4.46 2.01 |
0.703 0.215 0.557 0.004 0.956 0.003 0.471 0.035 0.157 |
Pain 2 h later | Age Sex Allergies Infection Delay since sting Number of spines Fish alive 1st time stung Time off work |
2.5 1.53 0.01 7.32 4.84 6.17 5.51 4.72 0 |
0.023 0.216 0.909 0.007 0.003 0.002 0.019 0.030 0.953 |
Analysis was performed using repeated ANCOVAs using the general linear model procedure whereby the reported pain score for each time point were dependent variables, and the following variables were analyzed as independent variables: age, sex, history of allergies, sting site infection, delay since sing, number of spines, fish alive, first time stung, and need for time off from work. F and P values were reported.
ANCOVA, analysis of covariance.
The number of spines from the lionfish that punctured the victim had a significant effect on the experience of pain. Overall, individuals stung by 3 or more spines experienced significantly more pain than those stung by 1 spine in our MMRM analysis (P = 0.0009, MMRM, see Fig. 2E). There was also a significant difference between the 1 spine and the 3+ spines groups at all time points except for immediately after the sting (P = 0.005, 0.002, <0.0001, and 0.003 at 1, 2, 24 hours and 1 week after the sting, respectively, ANCOVA analyses, see Table 6 and Supplemental Table 1, available at http://links.lww.com/PR9/A202).
Infection was a variable that was found to be globally statistically significant in our MMRM model (P = 0.0102, MMRM, see Fig. 2F) and was also statistically significant at all time points except for immediately after the sting (P = 0.033, 0.007, 0.007, and 0.004 for 1, 2, 24 hours, and 1 week after the sting, ANCOVA, see Table 6 and Supplemental Table 1, available at http://links.lww.com/PR9/A202).
Other factors that were statistically significant for certain time points in our ANCOVA model, but not in our MMRM model, included whether it was the first time that the individual had been stung and the delay between the sting and completion of the questionnaire. Prior experience with a lionfish sting proved to be a statistically significant variable at 2 hours, 1 day, and 1 week after the sting (P = 0.030; 0.036; and 0.035, respectively, ANCOVA model, see Table 6 and Supplemental Table 1, available at http://links.lww.com/PR9/A202). For these time points, prior experience with a lionfish sting tended to cause a reduction in the reported pain by the victim, whereas first-time sting victims tended to report significantly more pain. Of all the participants, 26.14% sought medical care or advice from a physician, nurse, or pharmacist (data not shown). Interestingly, individuals who needed to take time off from work because of the pain did not report significantly more pain than those who did not need time off (Table 6 and Supplemental Table 1, available at http://links.lww.com/PR9/A202).
4. Discussion
In this study, we provide the first large-scale study of the pain experience from lionfish stings. We assembled a questionnaire that may be used for other envenomations, including by other fish (eg, stonefish, scorpionfish), snakes, insects, and the like, to gain a wider understanding of the immediate pain and symptoms, as well as the impact of stings on the individual's life and work potential. We surveyed 555 individuals who have been stung by lionfish and obtained detailed information about the circumstances surrounding their sting, the conditions of their sting, the pain they experienced, and the interference the sting had on their personal lives.
By far, the most common activity that study participants were engaged in when they were stung by lionfish was spearfishing. This is not surprising considering that spearfishing requires a hunter to get close to the fish and to manipulate the fish with their hands to either remove them from their spear or empty their containment unit. Alarmingly, the invasion of the lionfish shows no sign of reversing soon,10,17 resulting in an increase in the number of individuals stung by lionfish in the future. Therefore, it is important to gain a better understanding of the consequences of lionfish envenomations, both from a physiological point of view and from a life-interference point of view.
Because anecdotal evidence has pointed to the fact that stings from dead lionfish produce less pain than from live ones, we asked participants to indicate whether the lionfish was alive at the time of their sting. In our ANCOVA model (Fig. 2B), we show that indeed live lionfish produce stings that produce more long-lasting pain than those of dead fish. This would confirm our group's prior findings that the algogenic toxin in the venom may degrade quickly, suggesting that it is proteinaceous in nature because this algogenic factor seems to degrade rather quickly after the fish's death.16
The most reported side effects of lionfish stings are pain, swelling, and redness with some experiencing paleness, bruising, blistering, and necrosis, in extreme cases; we sought to evaluate the frequency of these symptoms among the responders of our questionnaire. Indeed, pain, soreness, redness, and swelling were experienced by the majority of our participants, with paleness, bruising, blistering, and necrosis being experienced by less than 15% of our participants. This finding confirms anecdotal evidence presented in the literature based on case studies of lionfish stings.12,14,24,27
The exact time course of the pain caused by lionfish stings varies greatly, with some experiencing pain for a matter of minutes and others experiencing pain for weeks. Using the NIH PROMIS Short Form Pain Intensity Questionnaire, we characterized the time course of the pain experienced by sting victims. Our results showed that lionfish stings produce a moderate to significant amount of pain immediately after the sting, increasing until it reaches its peak at approximately 1 hour after the sting and reducing for the days following, healing completely within a week for most sting victims (Fig. 2). This pain varied based on the age of the victim, the number of spines they were stung by, whether the fish was alive or dead, and whether the site of the sting ultimately got infected. Importantly, however, the pain reported by victims did not vary based on sex (Fig. 2 and Table 6).
Because a prior study by our group indicated that lionfish venom activates nonpeptidergic nociceptors to cause pain, we sought to characterize whether the pain matched symptoms associated with neuropathic pain.16 To evaluate this, we used the self-reported portion of the DN4 questionnaire. Because the traditional cutoff for patients to be considered was 3,4,18 we concluded that the pain caused by lionfish venom in this case did not match the qualities of traditional neuropathic pain. This was somewhat expected because venoms are cocktails of molecules that often contain components which, in addition to components that activate nociceptors directly, trigger inflammatory reactions to amplify pain and discomfort in sting victims.2,5,7,25
Because of the intensity of the pain caused by lionfish stings and the fact that they tend to occur on hands, we hypothesized that this would lead to a highly disruptive experience for sting victims. We sought to quantify the degree of this disruption using the BPI Interference item. The maximum possible score for this item is 70 and is quantified from 0 to 10 in 7 different categories: general activity, normal work, mood, walking ability, sleep, enjoyment of life, and social activities. The mean total interference score in our study was 17.40/70 (±15.91) (Table 4). For comparison, the mean interference core associated with osteoarthritis pain is approximately 67.29 These results would suggest that although lionfish stings do not completely interfere or alter one's normal activities, a lionfish sting does pose a nuisance to its victims. In addition, more than two-thirds of the participants (69.37%) reported having needed to take time off from work because of their lionfish sting, reporting on average 17.98 (±17.33) hours of work missed. This would suggest that although lionfish stings pose a nuisance to everyday life, they also cause an average of approximately 2 missed workdays.
To determine whether pain from lionfish stings decreases as an individual gets stung more and more often, we asked participants to characterize whether the pain from the latest sting was less, the same, or more intense than the pain they experienced with past stings. In our ANCOVA model, we found that prior experience with a lionfish sting resulted in less pain for sting victims at the 2-hour time point and beyond. Thus, it seems that either prior experience with lionfish stings sets better expectations vis-à-vis the outcomes, producing less fear in victims of sting and ultimately resulting in less pain, or perhaps there exists some habituation mechanism that can be built by multiple exposures to lionfish venom.
Overall, pain-related questionnaires are very uncommon for victims of stings, and those that exist lack the line of questioning seen in comparable pain questionnaires, ultimately making it hard to compare results with existing pain data. The line of questioning followed in our study can be generalized to virtually any sting experience with some adaptation and would surely be beneficial for gaining insights into pain caused by stings and envenomations as well as the surrounding consequences of suffering from stings.
Government authorities are becoming increasingly aware of the damages caused by the invasion of the lionfish, especially on the local fish industries. Consequently, several initiatives have been set in place to help counter the impact of this invasion. Although it is known that individuals stung by the lionfish spines experience extreme pain, there remained several unknowns about the nature of the pain and how it affected the daily lives of the victims. In this study, we designed a clinical pain questionnaire that addressed these unknowns and have uncovered the important details on pain experience of individuals stung by lionfish, the risk factors that result in increased pain, and the extend of the interference of this pain on daily activities and work disability. These data not only will inform the general community to the risks associated with diving in lionfish-infested waters but also help in informing the medical community on the pain experience caused by a lionfish sting. Finally, these findings can also be used by local authorities to better appreciate the medical impact of the lionfish sting to further invest or develop new programs aimed at curtailing the expansion of the lionfish.
Recall bias remains a limitation of our study because participants may not have an exact memory of the pain they experienced at the time of their sting. Furthermore, the distribution of our questionnaire (throughout groups we knew had experience with lionfish stings) may have biased the demographics of our questionnaire to individuals in the southern states of the United States. Finally, the nature of the responses we received in this questionnaire were self-reported, thus potentially increasing overall variability between questionnaire participants or slightly overestimating reported pain.3,21
In conclusion, we have assembled the first large-scale study of the pain produced by lionfish stings. Data from our questionnaire have shown that victims of lionfish sting experience the peak of their pain approximately 1 hour after the sting and that most of the pain resolves itself around 7 days after sting. A variety of factors influence the intensity of the pain a victim will experience after being stung, including age, whether the fish was alive, the number of spines involved in the sting, infection, and prior experience with a lionfish sting. Taking all of these into account, we have provided novel insights into the nature of the pain, as well as which groups are likely to suffer more intensely from a lionfish sting and which factors correlate with elevated pain in victims of sting.
Disclosures
R.S.N. and S.M.C. have a startup company that developed a cream to treat the pain from the lionfish envenomation. M.C. declares no conflict of interest.
Appendix A. Supplemental digital content
Supplemental digital content associated with this article can be found online at http://links.lww.com/PR9/A202.
Supplementary Material
Acknowledgments
This study was supported by a CIHR project grant to R.S.N. and a Vanier Scholarship to S.M.C. The authors thank Mr. Marc Dorais (StatSciences) for consultation in biostatistics. S.M.C. and M.C. designed the questionnaire, S.M.C. analyzed the data, M.C. supervised the data analysis, R.S.N. and S.M.C. conceived the project, R.S.N. funded the study, S.M.C., M.C. and R.S.N. contributed to the writing of the manuscript.
Data availability statement: The authors are happy to make the data available upon request.
Footnotes
Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www.painrpts.com).
Contributor Information
Stephanie Mouchbahani-Constance, Email: stephanie.mouchbahaniconstance@mail.mcgill.ca.
Manon Choinière, Email: manon.choiniere@umontreal.ca.
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