A Scoping Review of the Respiratory Effects of Red Tide

Abstract

Algal blooms of Karenia brevis produce brevetoxins that lead to the natural phenomenon of red tide. Beyond monitoring the red tide concentration and forecasting future outbreaks, uncertainty exists in the field when examining these toxins in relation to the physiology of people. Contaminated air that results from outbreaks of K. brevis leads to inhalation of aerosolized brevetoxins, which directly impact the human respiratory system. This scoping review focused on the respiratory effects of red tide and was conducted by using a comparative method between 2 researchers. Relevant abstracts were collected, and full-text articles were reviewed by using PubMed, Science Direct, CINAHL Complete, and BioMed Central databases. Thirty articles were included in the final analysis and categorized by study design, location, and number and age of participants, and were also divided into assessment by respiratory effects, exposure, measurements of K. brevis, and asthma. The research indicates that respiratory health issues exist and can be compounded with exposure to red tide, specifically upper respiratory symptoms. Both symptomatic issues and pulmonary function tests were of concern when individuals were subjected to brevetoxin exposure. Even low levels of K. brevis resulted in negative respiratory health effects. Red tide is common in many areas of the world. The toxins released can cause adverse respiratory effects. This article provides a comprehensive summary of the scholarly literature focused on the respiratory system and red tide produced by K. brevis.

Introduction

The phenomenon known as red tide is the accumulation of algae that results in harmful algal blooms, which discolor affected waters and results in an increase of the marine dinoflagellate Karenia brevis.¹ In certain areas of the world, the marine dinoflagellate K. brevis creates harmful algal blooms that can cause unfavorable environmental conditions and ill effects in people.^1,2 Although the blooms commonly occur from late summer to early fall, progressively warming waters from a rapidly changing climate have resulted in increased frequency and intensity of blooms.^3-6 Harmful algal blooms of K. brevis have been reported along the Gulf of Mexico and have impacted all 5 gulf-coast states, although most notably in Florida. K. brevis blooms produce airborne marine particles that contain harmful brevetoxins, which can lead to negative health effects in humans.^2,7,8

Although these biotoxins can have an impact on the marine ecosystem, human adverse general health effects are seen when toxins enter through the skin and gastrointestinal system, harming both the nervous system and red blood cell production.^9-11 Emergency department admission rates of selected gastrointestinal diagnoses (gastritis, duodenitis, and non-infectious enteritis and colitis) have been found to be greater during a Florida red tide bloom period compared with a non-bloom period.¹² An increased incidence of headaches in individuals ages > 55 years in 6 southwest Florida counties during a K. brevis bloom has also been observed.¹³ Furthermore, K. brevis contains hemolytic compounds that increase toxicity levels and have negative implications on general human health.^14,15

From a respiratory perspective, the inhalation of brevetoxins present as a more concerning route of entry, triggering both upper and lower respiratory symptoms, such as shortness of breath, cough, bronchoconstriction, and asthma episodes and/or attacks.^1,3 These symptoms can be concerning to health-care providers who work in urgent care facilities during K. brevis blooms. Beyond monitoring K. brevis concentrations and forecasting future outbreaks, this study provides what data exist in the field when examining these toxins in relation to physiologic aspects of humans and the respiratory system. To the best of our knowledge, this literature review is the first scoping review published with regard to K. brevis red tide specifically focused on the respiratory effects. The objective of the research study was to synthesize current literature with regard to K. brevis, providing a summary of how environmental factors during red tide outbreaks of this dinoflagellate affect the human respiratory system.

Review of the Literature

Search Strategies

Red tide and respiratory effects peer-reviewed articles were identified from PubMed, ScienceDirect, CINAHL, and BioMed Central databases. A librarian was consulted to determine the best use of search terms and relevant literature in the field. The advanced search terms “red tide and resp*,” “algal blooms and k*brevis and resp,” “brevetoxins and lung,” “aerosolized red tide and respiratory irritation,” “air quality and red tide,” and “harmful algal blooms and public health” were used.

Eligibility

Retrieval of peer-reviewed articles was conducted by using a comparative method between 2 researchers (MED, TEO). Preferred Reporting Items for Systematic reviews and Meta-Analyses 2020 statement guidelines were followed to deem articles eligible for inclusion. Inclusion criteria consisted of full-text articles in English related to humans and the respiratory effects of red tide. There were no date limitations in this study. Exclusion criteria were any articles not pertaining to red tide and respiratory effects, animal studies, or reviews, or those that were not written in the English language. The initial search yielded 4,529 abstracts. Abstracts that could not be categorized based on a lack of information were reviewed in full text before exclusion from the data. Before full-text screening, omitted abstracts included those that did not meet the inclusion criteria. Of the 1,349 full-text articles screened, 1,280 were subsequently excluded. This lack of fit included using subjects other than humans, the inclusion of cyanobacteria data, and findings unrelated to the respiratory system. With the 69 remaining articles, full text articles were reviewed a second time to determine eligibility. Thirty-nine articles were excluded based on inclusion of cyanobacteria instead of red tide, duplicates, and animal studies. A final 30 articles were included in this scoping review.^{2,5,7,8,12,16-40} (Figure 1).

Fig. 1.

Flow chart.

Results

The data in the current study represent a scoping review of K. brevis red tide and its respiratory effects. A summarization of the retrieved studies was performed below for the study design, location of study data collection, demographic information, and the methods of data collection. In relation to study design, there was found to be one ecologic study,³⁶ 12 experimental studies,^{7,12,17,18,22,26,27,31,32,37-39} 5 observational studies,^{2,20,21,25,29,} 5 prospective cohort studies,^{1,19,24,28,40,} one case report,³⁰ 2 cross-sectional studies,^8,23 one retrospective cohort study,¹⁶ one pre-post study,³⁴ and one crossover study.³⁵ Of the 30 studies, 21 involved both participants and data collected in Florida,^{1,2,7,8,12,16-21,23-25,27,28,30,34-36,40} one study involved participants located in Christi Corpus, Texas,³⁹ one study involved participants both in Florida and Texas,³⁷ and one study involved participants located in North Carolina.³³ Three studies were located outside of the United States.^22,26,38

Most of the studies involved male and female participants 12–65 y old. Study methods varied between data collection of respiratory effects and brevetoxin exposure. Most of the experimental studies focused on aerosol samples of brevetoxins, determining where in the human respiratory tract particles of brevetoxins are able to deposit. Methods of collection in relation to symptoms included questionnaires, nasal swabs, and spirometry readings. Detection of brevetoxins in the nasal swab indicates that brevetoxins have the potential to be deposited in the respiratory tract on participants.¹⁷ Furthermore, we summarized the articles by exposure, respiratory effects, brevetoxin specifics, and relationship to asthma.

With regard to respiratory effects, most of the studies indicated some type of respiratory irritation such as nasal congestion, throat irritation, and cough after exposure to brevetoxins.¹² In a comparison between upper and lower respiratory symptoms, there is a more prominent association between brevetoxin exposure and reports of upper respiratory symptoms.^1,12,36 These respiratory symptoms included sore throat, coughing, nasal congestion, and sneezing.^1,25,35,36 However, both upper and lower respiratory symptoms related to biotoxins from aerosolized K. brevis blooms were seen throughout the studies and included wheezing, shortness of breath, chest tightness, coughing, and nasal and throat irritation.^{16-19,25,29,30,34-36} When analyzing respiratory effects via spirometry, one study found with highly variable average peak flow volumes after exposure on the beach.³⁵ Increased emergency department admissions for respiratory-related issues were higher in the months with blooms versus months without blooms One article found an association with K. brevis exposure and emphysema.³⁶ Articles that pertain to respiratory-related effects are provided in Table 1.

Table 1.

Respiratory Symptoms From Karenia brevis

Exposures throughout the calendar year or among seasons, with exposures measured highest in both spring and fall months.^1,37 One study did not find differences in exposure among demographic variables.³⁶ Low exposure levels can lead to respiratory issues. Individuals working and living on beaches experienced higher exposure.^16,35 It was found that, when K. brevis was present, there were uniform exposure levels across the beach, from near the surf to 50 m onto the beach.¹ Articles that pertain to exposure are provided in Table 2.

Table 2.

Exposure to Karenia brevis

Methods of data collection in relation to brevetoxins included high-volume air samplers, microscopy identification, liquid chromatography mass spectrometry, and brevetoxin enzyme-linked immunosorbent assay. In a particular study, detection of brevetoxins in the nasal swab of participants indicated that brevetoxins are inhaled and that the nasal airway is the primary target for these toxins.¹⁷ Furthermore, during relatively high amounts of red tide, 68% of nasal swabs showed greater detectable levels of brevetoxins. To fully comprehend findings within the research, once particle size of brevetoxins was found in both the exposed and nonexposed study groups with a lung model used to estimate the deposited dose of particles in different regions of the respiratory tract.³⁶ One study also included yessotoxins and found extremely low concentrations of harmful algal blooms compared with brevetoxin (PbTx).¹⁸ The biotoxin that was most prevalent in the included studies was PbTx.^{7,22,31,37,39} Studies that collected particle size data of airborne PbTx found a size range of 2.8 to 5 ng/m³, which indicates a high deposition in the upper respiratory tract.^7,37 Articles specific to brevetoxins are provided in Table 3.

Table 3.

Results Related to Brevetoxin Concentration

In general, asthma exacerbations do exist with exposure to K. brevis because even low levels result in respiratory symptoms.⁴⁰ In a study with 7 participants (5.4%) with previously diagnosed asthma during the low- and high-exposure period, there was no report of an increase in symptoms. In the moderate exposure group, one participant with asthma reported lower respiratory irritation, whereas 2 participants with asthma reported upper respiratory symptoms.¹⁷ Most studies reported only acute symptoms such as cough, wheezing, chest tightness, and throat and/or eye irritation, and found that asthma symptoms increase as exposure to red tide toxins increases.^{1,12,19,32,40} One study supported the concept that brevetoxins may trigger asthma through stimulation of cholinergic nerve fiber sodium channels.³¹ A single study in this review followed up a cohort of participants with stable asthma who were living in areas with intermittent Florida red tides, and the participants did not exhibit chronic respiratory effects over time from exposure to brevetoxins.⁴⁰ The asthma-related articles are provided in Table 4.

Table 4.

Results Related to Asthma

Discussion

This article focused on a review of the respiratory effects of K. brevis. This finding is consistent with most other studies and could relate to the particle size found in nasal airways. Our studies focused on respiratory-related health effects and exposure related to K. brevis. Other studies differ in that they have focused on the mechanisms of the observed bronchoconstriction. In a laboratory experiment that researched³² the specific human airway smooth muscle in relation to PbTx, vascular organ donors were labeled as either having asthma or not having asthma to assess depolarizations when exposed to brevetoxins. The researchers induced change in the electrical charge to better understand the smooth-muscle contraction in relation to exposure with brevetoxins as well as understanding that the bronchoconstriction experienced when individuals are exposed environmentally to PbTx supports the depolarizing effect of endogenous acetylcholine, inducing the toxic effect in asthma airways.²⁷

Emergency department visits were used as a measure throughout the studies included in this review. In comparative research findings, residents living in coastal areas during K. brevis blooms experienced hospital admissions for respiratory diseases compared with digestive diseases.^16,21,29 There are clear limitations within our collected studies, which include self-reporting of symptoms, no information with regard to medications used before and after red tide in participants with asthma, and time variances of exposure based on study design.

Future research should continue to follow cohorts of both individuals with asthma and those without asthma who were living near K. brevis bloom–prone areas in assessing potential chronic respiratory effects. Continued research that monitors the specific type of brevetoxins during active K. brevis red tide blooms can aid in assessing potential associations and a correlation between toxin profile and a known correlation with the respiratory system. Furthermore, understanding what is reported in the scholarly literature will be valuable and informative for respiratory therapists and pulmonary health-care providers who live in areas prone to K. Brevis blooms.

Summary

The prevalence of red tide and its threat to many coasts of the world produces concerns as a potential for respiratory health issues. Published literature has established that the severity of respiratory effects experienced by humans is primarily dependent on exposure and concentration of aerosolized brevetoxins. Understanding the effects of red tide on the respiratory system can aid in both health management practices and education. Public health campaigns with regard to the effects of red tide may aid in increasing awareness and in providing prevention education. Hospitals should also consider being a venue for educational information, particularly in states prone to K. brevis outbreaks.