Economic impact of harmful algal blooms on human health: a systematic review

Harmful algal blooms (HABs) damage human activities and health. While there is wide literature on economic losses, little is known about the economic impact on human health. In this review, we systematically retrieved papers which presented health costs following exposure to HABs. A systematic review was conducted up to January 2019 in databases such as ScienceDirect and PubMed, and 16 studies were selected. Health costs included healthcare and medication expenses, loss of income due to illness, cost of pain and suffering, and cost of death. Two categories of illness (digestive and respiratory) were considered for health costs. For digestive illness cost, we found $86, $1,015 and $12,605, respectively, for mild, moderate and severe cases. For respiratory illness, costs were $86, $1,235 and $14,600, respectively, for mild, moderate and severe cases. We used Quality-Adjusted Life Years (QALYs) to access the loss of well-being due to illness caused by HABs. We found that breathing difficulty causes the most loss of QALYs, especially in children, with a loss of between 0.16 and 0.771 per child. Having gastroenteritis could cause a loss of between 2.2 and 7.1 QALYs per 1,000 children. Misleading symptoms of illness following exposure to HABs could cause bias in health costs estimations. This is an Open Access article distributed under the terms of the Creative Commons Attribution Licence (CC BY 4.0), which permits copying, adaptation and redistribution, provided the original work is properly cited (http://creativecommons.org/licenses/by/4.0/). doi: 10.2166/wh.2019.064 s://iwaponline.com/jwh/article-pdf/17/4/499/644647/jwh0170499.pdf Christian R. C. Kouakou Thomas G. Poder (corresponding author) Department of Economics, University of Sherbrooke, Sherbrooke, Montreal, Canada E-mail: thomas.poder@usherbrooke.ca Thomas G. Poder Department of Management, Evaluation and Health Policy, School of Public Health of the University of Montreal, University of Montreal, Montreal, QC, Canada This article has been made Open Access thanks to the generous support of a global network of libraries as part of the Knowledge Unlatched Select initiative.


INTRODUCTION
Harmful algal blooms (HABs) produce toxins that can adversely affect human health (Backer & McGillicuddy ; Figgatt et al. ). Human exposure to harmful algae can occur in many ways (Otten & Paerl ), i.e., through recreational water (direct or indirect contact), drinking contaminated water, or consuming food (e.g., fish Despite the known toxicity of harmful algae, the consumption of some algae (i.e., cyanobacteria) is voluntary in some cases (i.e., blue-green algae supplements) mainly due to their high protein content and some health benefits (e.g., detox, elevated mood and energy, increased alertness and vivacity)  Table A1 in Supplementary Material, available with the online version of this paper).

Studies' selection
In our documentary research protocol, the selection of studies was based on these criteria: • Studies (e.g., article, review, report, and note) connected with HAB, blue-green algae, toxins, or cyanobacteria.
• Studies including health episodes, public health costs, and healthcare costs.
• Studies including an effect on health-related quality of life.
Excluded studies were those that did not include health effects (e.g., only environment and tourism). We excluded studies about the waterborne or foodborne disease which did not specifically talk about harmful algae.
The first selection of studies was made after two evaluators read the titles and summaries. Studies selected at this stage were then read in full and only kept if they met the inclusion criteria. We had no restrictions on the target population. Data extraction was done by an evaluator and validated by a second. In case of discrepancy in the data collected, a call to an arbitrator was made.
The main information we sought to collect was symptoms related to disease, frequency of healthcare consumption (e.g., consultation, emergencies, and medication), expenses related to these health episodes and the resulting loss of health-related quality of life (e.g., QALY).

Data analysis
We did a descriptive analysis of the data. Cost data were extracted and then capitalized in 2016 US dollars. If an article did not specify the year of reference for the costs, the article's year of publication was considered the reference year. For the capitalization of costs in 2016 US dollars, we used the price index available in the World Development Indicators (WDI) database of the World Bank (WB). Symptoms were grouped according to the major categories. Then, we described health episodes in terms of consultation, care, and medical monitoring. Costs associated with healthcare were calculated based on data available and the size of the sample concerned.
As appropriate, we reported the data per case, per day of sickness, or per kilometer of coastline. The quality of each study was evaluated by a grid. We used the NIH Quality Assessment Tool to evaluate primary studies (NHLBI ), AMSTAR for literature reviews (Shea et al. ), and the grid AGREE II for reports (Brouwers et al. ).

Studies' selection
The PRISMA flow diagram ( Figure 1) presents a detailed process for selecting the articles in our systematic review.
In total, 1,524 articles were identified, and 69 were read in full to evaluate their eligibility. Ultimately, 16 studies were selected to include in this review. The reason for excluding studies that were fully read was as follows: studies reported waterborne diseases only without cost data (n ¼ 22) or general waterborne disease without linking with harmful algae (n ¼ 4); studies reported economic cost but not for health (n ¼ 6); study reported willingness to pay for harmful algae health hazard reduction (n ¼ 1); studies reported general impact (e.g., biological and ecological) of harmful algae (n ¼ 9); studies reported ocean pollution (n ¼ 2); studies reported seafood contamination (n ¼ 5) and cost of foodborne disease (n ¼ 2); study reported health episode and cost data for general waterborne illness (n ¼ 1); and study valuing protection against invasive marine species (n ¼ 1).

Characteristics of studies included
Three main types of studies were identified as primary studies (n ¼ 9) (Table 1), literature reviews (n ¼ 2) (Table 2), and reports (n ¼ 5) (Table 3). Most studies were about the United States (n ¼ 13), some on the European Union (n ¼ 2) and Canada (n ¼ 3), and two were about Pacific Ocean Islands (French Polynesia and the Cook Islands).
Data were all published in the 2000s except one study in 1995. The studies focused most often on harmful algae, without specifying the type of algae. When reported, the source of water was coastal or salt water (n ¼ 10) and freshwater (n ¼ 2). While some studies focused on costs at a national level, other costs were by the cause of illness or sick day.

Symptoms developed
The studies retrieved in this review contain cost data related to health issues following contamination by harmful algae.
However, most of the studies do not show explicit information about symptoms developed and subsequent health episodes. This precludes documenting the impact of HABs on health-related quality of life. To document more exhaustively these symptoms and better understand their typology, we had to complete our list with additional studies. These studies were collected from the list of full-text articles assessed for eligibility. The studies selected were those that reported diseases and health episodes due to exposure to cyanobacteria and HABs. We grouped the symptoms identified into six major groups, adapted from Hilborn et al.
(), and the last one which concerns death (Table 4).
Symptoms are related to the type of contact with con- people died from a deficiency of the liver after receiving hemodialysis treatment with cyanotoxin-contaminated water. People who had indirect contact (e.g., inhalation of water spray) with water had a higher risk, probably because they did not take sufficient protection measures (Lévesque ).
Besides the symptoms that generally develop as a result of direct or indirect contact with water, the literature also presents cases of diseases following the consumption of These cases were determined based on a combination of official data (Health and Welfare Canada) and hypotheses established by experts (Todd , a, b, c, ).
In addition, long-term (chronic) effects such as liver cancer, colorectal cancer, and even death because of chronic harmful algae exposure are cited in the literature    to the cost of absenteeism, which the authors defined as missed hours of work due to illness or medical conditions.
The cost of absenteeism consisted of the cost of medical treatment and the cost of lost productivity due to the illness. They also estimated the cost of presenteeism, such as the amount

Costs of disease
In general, and according to studies, health costs can be categorized into three subgroups of costs: (direct) healthcare

Short-and long-term costs
All the studies included only assessed costs related to acute exposure to HABs that is short-term costs observed in a relatively short period (days or weeks). No studies included costs on a long-term basis, such as costs related to chronic exposure to HABs or chronic illness that may be caused by chronic exposure to contaminated water.

Other costs
The costs of investigating sickness could also be considered in the accounting of the overall costs related to exposure to HABs. Time spent interviewing patients, epidemiological analysis of data, communication with other services and writing reports for a total estimated at $697 per case of illness, and laboratory examination costs ranged from $278 to $556 (Todd ).

Impact on health-related quality of life
In this section, we show data on health-related quality of life for the illnesses reported in Table 4. The aim was to give an insight into how much well-being one (or a society) could lose when facing these illnesses, which may be caused by HABs. We found that breathing difficulty appeared to be the sickness which caused the most loss of QALYs in children, with a loss ranging between 0.16 and 0.771 per child We carried out calculations to assess the overall burden of diseases caused by HABs. We retained two illnesses (respiratory and digestive) and death, three levels of severity (mild, moderate and severe) and 3 days of the disease,

DISCUSSION
Overall, reviewing the literature to address the lack of health cost data and trying to put together all these studies which had potential interest for our review led to some concern.
Unreported illness could be, by far, the most important The misleading symptoms of illness following exposure to harmful algae are also a limit. Since having flu, headache, diarrhea or fatigue, and the like may not be caused only by exposure to harmful algae; it is difficult to establish a direct and causal relationship between observed symptoms and  There is an incapacity to measure all the costs following exposure to harmful algae, e.g., the cost of pain and suffering. Most of the studies included in our review did not consider these kinds of cost. One study (Nierenberg et  We included studies which met our inclusion criteria without considering their methodological rigor since most were of low quality. This may be kept in mind while considering the overall results of this review. While extracting and reporting the cost data from the studies, some did not report explicitly the years in which costs are expressed. So, for the studies that did not give the year of their costs, we assumed the cost for the year of publication. The QALYs reported in Table 6 were not measured with the same tool. We had no means to make the correspondence between them. However, this provides an idea of these costs. Overall, the quality of the studies included in this review is moderate, especially for primary studies, even if reviews and reports did not match all the criteria well. Some studies were based on a population which may be concerned about water pollution, and extrapolation of the results may be done with precaution. Illness from shellfish presented by Todd () concerned sporadic events across Canada; this is the case for Hoagland et al. (). Since it remains difficult to collect data over all the contamination cases, all studies included in this review collected data on the same population or in the same time period. This may be a concern which should be considered when it comes to generalizing the results. The fact that not all the studies are precise about the harmful algae considered creates uncertainty over to which algae one could attribute the illness. However, it would not be easy to isolate the effect or contribution of each algae species on the disease. Finally, we found no specific study about cyanobacteria, and little is known about their impact on health and related health expenses (Donohue et al. ).
Finally, the fact that some studies used survey and selfreported exposure and illness could create a bias in the data used for cost estimation. In fact, having contact with water did not necessary imply contamination by HA as well as having symptoms similar to those caused by algae.
In the absence of a medical diagnostic, self-reported data should be considered with caution.

CONCLUSION
This review gave specific regard to the economic impact of harmful algae on human health. We found that harmful algae could cause many health problems and generate important expenses. Having more studies which focus on the health aspects and consequences of human health could help present a better understanding of these health problems. Although this study may have some weakness due to the quality of the selected studies, it remains methodologically rigorous and could help assess human health costs due to cyanobacteria and harmful algae in general.