## Abstract

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 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 2006; Figgatt et al. 2016). Human exposure to harmful algae can occur in many ways (Otten & Paerl 2015), i.e., through recreational water (direct or indirect contact), drinking contaminated water, or consuming food (e.g., fish and contaminated seafood) (Vasconcelos 1999; de Magalhaes et al. 2001; Lee et al. 2017). Potential health problems vary and strongly depend on the level of exposure to the source of contamination (Bláha et al. 2009). The main problems encountered are gastroenteritis, abdominal pain, nausea, vomiting, diarrhea, muscle aches, fever, liver, kidney, and intestinal damage, and more (Chorus et al. 2000; Koreivienė et al. 2014; Wood 2016; Svirčev et al. 2017). Cases of death were reported following dialysis with contaminated water (Jochimsen et al. 1998; Carmichael et al. 2001; Azevedo et al. 2002) or after the consumption of contaminated water (Teixeira et al. 1993).

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) (Dietrich & Hoeger 2005; Drobac et al. 2013; Ananya & Ahmad 2014). However, some authors found that some algae dietary supplements contained ‘cyanotoxins at levels exceeding the tolerable daily intake values’ (Roy-Lachapelle et al. 2017). Beyond the direct health consequences, HABs also have an impact on recreational activities by degrading the esthetic quality of recreational waters' coloring and producing a bad smell (Dodds et al. 2009; Carmichael & Boyer 2016), which can affect the quality of life for residents.

The literature is full of articles relating the health consequences of exposure to harmful algae (Pilotto et al. 1997; Osborne et al. 2007; Hilborn et al. 2014; Lévesque et al. 2014, 2016). However, fewer are those reporting the economic consequences related to health (e.g., costs of care, economic impacts, and quality of life). This systematic review aims to report the costs and health economic consequences of contamination episodes by harmful algae including cyanobacteria. Precisely, this review aims to document the monetary costs of contamination episodes (i.e., medical consultation, hospitalization, emergency visits, drug expenditures, and loss of productivity) and the impact on health-related quality of life. We chose to do a systematic review of the literature on this topic since it is an effective way to inform decision-makers and help them make a decision based on reliable evidence (Bennett et al. 2018).

## METHODS

### Research strategy

Databases consulted were Medline EBSCO, Scopus, ScienceDirect (Elsevier), PubMed, and the Cochrane Library. A search in the gray literature was carried out via Google, Google Scholar, and the websites of the public health agencies of Canada and Quebec. We also consulted the bibliographical references of the selected articles to collect additional relevant references. Keywords used for research were HAB, harmful algal bloom, toxin, cyanobacteria, blue-green algae, health, economic, economics, cost, QALY, and Quality-Adjusted Life Year. With the Boolean operators ‘AND’ and ‘OR,’ we made combinations between the keywords to get closer to the desired meaning. We also performed a search with the entire title of our article (‘Economic impact of harmful algal bloom and cyanobacteria on human health’) in Google and Google Scholar. No language or date restrictions were used. The search was carried out in English in the databases named above, then in English and French in Google, Google Scholar, and the public health agencies' internet pages. The search ended on 7 January 2019 (see 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 2014), AMSTAR for literature reviews (Shea et al. 2007), and the grid AGREE II for reports (Brouwers et al. 2010).

## RESULTS

### 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 = 22) or general waterborne disease without linking with harmful algae (n = 4); studies reported economic cost but not for health (n = 6); study reported willingness to pay for harmful algae health hazard reduction (n = 1); studies reported general impact (e.g., biological and ecological) of harmful algae (n = 9); studies reported ocean pollution (n = 2); studies reported seafood contamination (n = 5) and cost of foodborne disease (n = 2); study reported health episode and cost data for general waterborne illness (n = 1); and study valuing protection against invasive marine species (n = 1).

Figure 1

PRISMA flow diagram for the selection of studies, 7 January 2019.

Figure 1

PRISMA flow diagram for the selection of studies, 7 January 2019.

### Characteristics of studies included

Three main types of studies were identified as primary studies (n = 9) (Table 1), literature reviews (n = 2) (Table 2), and reports (n = 5) (Table 3). Most studies were about the United States (n = 13), some on the European Union (n = 2) and Canada (n = 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 = 10) and freshwater (n = 2). While some studies focused on costs at a national level, other costs were by the cause of illness or sick day.

### Symptoms developed and health episodes

#### 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. (2014), and the last one which concerns death (Table 4).

Table 1

Characteristics of studies included (primary studies)

Authors (year)
country
Data sourceWater source/algae types or toxinsSymptoms/observationsEstimated costs for healthCost typeQuality of the study (NIH)
Todd (1995)
Estimated by the author Coastal water (saltwater)/not specified Illnesses from seafood $590 K annual for 525 cases, or$1,124 per case of foodborne poisoning by harmful algae
$500 K for death Illness cost for a person eating seafood. No value attributed to pain, grief, or suffering 6/14 Hoagland et al. (2002) United States Survey of experts, review of literature, authors' calculation Coastal water (saltwater)/not specified Shellfish poisoning, ciguatera fish poisoning Approximately$20M per year nationwide ($2000) Hospitalization, investigation, productivity loss and death 9/14 Hoagland & Scatasta (2006) European Union and United States Data from published and unpublished studies Coastal water (saltwater)/not specified Shellfish poisoning, ciguatera fish poisoning$11M for the European Union and $37M for the USA, per year ($2005) Updated cost from Hoagland et al. (2002) and Anderson et al. (20007/14
Hoagland et al. (2009)
Florida (United States)
Department of Emergency Sarasota Memorial Hospital and US Census Bureau Coastal water (saltwater)/Karenia brevis Respiratory illnesses $0.52M–$4.18M over 5 years for Sarasota County only ($2008) Emergency department visits and productivity loss 10/14 Hoagland et al. (2014) Florida (United States) Florida Agency for Health Care Administration, Florida Department of Agriculture and Consumer Services, US Census Bureau Coastal water (saltwater)/Karenia brevis Respiratory illness, digestive illness$60 K–$700 K annually for Florida ($2013) Treatment cost (emergency visit, hospital admission) and lost incomes during both treatment and recuperation 9/14
Morin et al. (2016)
French Polynesia
Survey, hospital data, literature Lagoon (fresh water) Ciguatera fish poisoning $1,613 for each reported case and$749 for each unreported case $1,146 overall for each case (reported or unreported) ($2016) Hospitalization fees, medication fees, cost of non-productive days 7/14
Rongo & van Woesik (2012)
Southern Cook Islands
Survey, ministry of health, local pharmacists, statistics office Lagoon (fresh water) Ciguatera poisoning $1,400 for an individual with ciguatera poisoning Hospital and staff time involved in the treatment, price of pharmaceuticals, lost labor productivity 8/14 Nierenberg et al. (2010) Florida (United States) Beach Lifeguard Survey, county public records, and a WTP study by Blackwell & Tunny (2000) Coastal water (saltwater)/Karenia brevis Absenteeism and presenteeism of rescuers due to illness Average cost of absenteeism estimated at$3,000. Presenteeism could be estimated at $82,772 ($2009) Productivity loss and cost of medical treatments 9/14
Ralston et al. (2011)
United States
Literature, surveillance and monitoring data and a cost-of-illness model from the USDA Coastal water (saltwater)/not specified All consequences (pathologies of marine origin, food, recreation) $900M annual for the whole of the United States, two-third by alimentary intoxication and one-third by direct contact Costs include lost wages, physician and hospital services, and statistical cost of premature death 9/14 Authors (year) country Data sourceWater source/algae types or toxinsSymptoms/observationsEstimated costs for healthCost typeQuality of the study (NIH) Todd (1995) Canada Estimated by the author Coastal water (saltwater)/not specified Illnesses from seafood$590 K annual for 525 cases, or $1,124 per case of foodborne poisoning by harmful algae$500 K for death
Illness cost for a person eating seafood. No value attributed to pain, grief, or suffering 6/14
Hoagland et al. (2002)
United States
Survey of experts, review of literature, authors' calculation Coastal water (saltwater)/not specified Shellfish poisoning, ciguatera fish poisoning Approximately $20M per year nationwide ($2000) Hospitalization, investigation, productivity loss and death 9/14
Hoagland & Scatasta (2006)
European Union and United States
Data from published and unpublished studies Coastal water (saltwater)/not specified Shellfish poisoning, ciguatera fish poisoning $11M for the European Union and$37M for the USA, per year ($2005) Updated cost from Hoagland et al. (2002) and Anderson et al. (20007/14 Hoagland et al. (2009) Florida (United States) Department of Emergency Sarasota Memorial Hospital and US Census Bureau Coastal water (saltwater)/Karenia brevis Respiratory illnesses$0.52M–$4.18M over 5 years for Sarasota County only ($2008) Emergency department visits and productivity loss 10/14
Hoagland et al. (2014)
Florida (United States)
Florida Agency for Health Care Administration, Florida Department of Agriculture and Consumer Services, US Census Bureau Coastal water (saltwater)/Karenia brevis Respiratory illness, digestive illness $60 K–$700 K annually for Florida ($2013) Treatment cost (emergency visit, hospital admission) and lost incomes during both treatment and recuperation 9/14 Morin et al. (2016) French Polynesia Survey, hospital data, literature Lagoon (fresh water) Ciguatera fish poisoning$1,613 for each reported case and $749 for each unreported case$1,146 overall for each case (reported or unreported) ($2016) Hospitalization fees, medication fees, cost of non-productive days 7/14 Rongo & van Woesik (2012) Southern Cook Islands Survey, ministry of health, local pharmacists, statistics office Lagoon (fresh water) Ciguatera poisoning$1,400 for an individual with ciguatera poisoning Hospital and staff time involved in the treatment, price of pharmaceuticals, lost labor productivity 8/14
Nierenberg et al. (2010)
Florida (United States)
Beach Lifeguard Survey, county public records, and a WTP study by Blackwell & Tunny (2000)  Coastal water (saltwater)/Karenia brevis Absenteeism and presenteeism of rescuers due to illness Average cost of absenteeism estimated at $3,000. Presenteeism could be estimated at$82,772 ($2009) Productivity loss and cost of medical treatments 9/14 Ralston et al. (2011) United States Literature, surveillance and monitoring data and a cost-of-illness model from the USDA Coastal water (saltwater)/not specified All consequences (pathologies of marine origin, food, recreation)$900M annual for the whole of the United States, two-third by alimentary intoxication and one-third by direct contact Costs include lost wages, physician and hospital services, and statistical cost of premature death 9/14

K, Thousand; M, Million.

Table 2

Characteristics of studies included (literature reviews)

Authors (year)
country
Number of studiesWater source/algae type or toxinsEstimated health costsQuality of the study (AMSTAR)
Fleming et al. (2011)
Florida (United States)
Two for the health costs section Coastal water (saltwater)/Karenia brevis Vary according to the studies from $3 K per case to$4M annually for the county of Sarasota (Florida) 0/11
Nine studies with health costs Not specified/various Vary according to studies from $100 K to$900M annually for countries (or regions) 3/11
Authors (year)
country
Number of studiesWater source/algae type or toxinsEstimated health costsQuality of the study (AMSTAR)
Fleming et al. (2011)
Florida (United States)
Two for the health costs section Coastal water (saltwater)/Karenia brevis Vary according to the studies from $3 K per case to$4M annually for the county of Sarasota (Florida) 0/11
Nine studies with health costs Not specified/various Vary according to studies from $100 K to$900M annually for countries (or regions) 3/11

K, Thousand; M, Million.

Table 3

Characteristics of studies included (reports)

Authors (year)
country
PopulationSymptoms/observationsEstimated costs for healthQuality of the study (AGREE II)
Anderson et al. (2000)
United States
United States Diseases caused by seafood, ciguatera, and undeclared diseases $18.4M–$25M annual ($2000) 3/7 Bauer (2006) United States United States Intoxication by the consumption of seafood and ciguatera$31.5M ($2000) 6/7 Andreatta et al. (2012) United States United States Not reported$37M ($2005) 4/7 USEPA (2015) United States Sarasota County, Florida Not reported$21 K–$138.6 K per year ($2012) 4/7
Sanseverino et al. (2016)
Canada, United States Not reported $20 K–$900M per year 3/7
Authors (year)
country
PopulationSymptoms/observationsEstimated costs for healthQuality of the study (AGREE II)
Anderson et al. (2000)
United States
United States Diseases caused by seafood, ciguatera, and undeclared diseases $18.4M–$25M annual ($2000) 3/7 Bauer (2006) United States United States Intoxication by the consumption of seafood and ciguatera$31.5M ($2000) 6/7 Andreatta et al. (2012) United States United States Not reported$37M ($2005) 4/7 USEPA (2015) United States Sarasota County, Florida Not reported$21 K–$138.6 K per year ($2012) 4/7
Sanseverino et al. (2016)
Canada, United States Not reported $20 K–$900M per year 3/7

K, Thousand; M, Million.

Table 4

Categories of symptoms developed because of exposure to harmful algae

SymptomsReferences
General Dizziness, muscle aches, fatigue, sore throat, discomfort, weakness, back pain, tingling, mouth ulcers Pilotto et al. (1997); Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); Lévesque et al. (2014); Figgatt et al. (2017)
Gastrointestinal Abdominal cramps, diarrhea, vomiting, nausea, gastroenteritis Teixeira et al. (1993); Pilotto et al. (1997); Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); MSSS (2014); Lévesque et al. (2014); Lin et al. (2016); Figgatt et al. (2017)
Skin Rash, swelling, sores, irritation, dermatological symptoms, itching, redness, burns Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); MSSS (2014); Lévesque et al. (2014); Lin et al. (2016); Figgatt et al. (2017)
Eye, ear Tearing, eye irritation, ear pain, visual disturbance, eye symptoms, flow from eyes and ears Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); Lévesque et al. (2014); Lin et al. (2016); Figgatt et al. (2016, 2017
Respiratory Nasal congestion, cough, wheezing, shortness of breath, chest discomfort, respiratory symptoms, cold, flu Pilotto et al. (1997); Lévesque (2009); Hoagland et al. (2009); Hilborn et al. (2014); MSSS (2014); Lin et al. (2016); Figgatt et al. (2017)
Fever and headache Fever, headache Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); Figgatt et al. (2017)
Death Death Teixeira et al. (1993); Jochimsen et al. (1998); Carmichael et al. (2001); Azevedo et al. (2002)
SymptomsReferences
General Dizziness, muscle aches, fatigue, sore throat, discomfort, weakness, back pain, tingling, mouth ulcers Pilotto et al. (1997); Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); Lévesque et al. (2014); Figgatt et al. (2017)
Gastrointestinal Abdominal cramps, diarrhea, vomiting, nausea, gastroenteritis Teixeira et al. (1993); Pilotto et al. (1997); Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); MSSS (2014); Lévesque et al. (2014); Lin et al. (2016); Figgatt et al. (2017)
Skin Rash, swelling, sores, irritation, dermatological symptoms, itching, redness, burns Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); MSSS (2014); Lévesque et al. (2014); Lin et al. (2016); Figgatt et al. (2017)
Eye, ear Tearing, eye irritation, ear pain, visual disturbance, eye symptoms, flow from eyes and ears Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); Lévesque et al. (2014); Lin et al. (2016); Figgatt et al. (2016, 2017
Respiratory Nasal congestion, cough, wheezing, shortness of breath, chest discomfort, respiratory symptoms, cold, flu Pilotto et al. (1997); Lévesque (2009); Hoagland et al. (2009); Hilborn et al. (2014); MSSS (2014); Lin et al. (2016); Figgatt et al. (2017)
Fever and headache Fever, headache Osborne et al. (2007); Lévesque (2009); Hilborn et al. (2014); Figgatt et al. (2017)
Death Death Teixeira et al. (1993); Jochimsen et al. (1998); Carmichael et al. (2001); Azevedo et al. (2002)
Table 5

Average health costs estimated following exposure to harmful algae

Cost per caseDescription of costsReferences
$1,770 Costs per case of illness because of food poisoning by algae (This cost includes societal cost, cost to the individual and different affected parties) Todd (1995)$787.5 K Cost per case of death
$1,951 Cost per case of reported illness Hoagland et al. (2002)$1,533 Cost per case of unreported illness
$1.4M Cost per case of death$207/km Cost per kilometer of coastline for the European Union Hoagland & Scatasta (2006)
$2,281/km Cost per kilometer of coastline for the United States$572–$586–$664 Min. cost – Avg. – Max. for a case of respiratory illness Hoagland et al. (2009)
$1,025–$2,160 Low and high cost per emergency department visit for RI and DI Hilborn et al. (2014)
$4,670–$15,620 Low and high cost per inpatient admission for RI and DI
$166 Daily cost of absenteeism per case of illness (cost-of-illness treatment and loss of productivity) Nierenberg et al. (2010)$253.7 Cost of presenteeism (WTP per beachgoer to have an additional lifeguard during the bloom period)
$64 Cost per case of gastroenteritis due to direct contact with water Ralston et al. (2011)$130 Cost per case of illness due to food poisoning
$5.3M Cost per case of death$1,613 For each reported case Morin et al. (2016)
$749 For each unreported case$1,146 Mean cost for each case (reported or unreported)
$1,464 For each reported case Rongo & van Woesik (2012)$423 For each unreported case
Cost per caseDescription of costsReferences
$1,770 Costs per case of illness because of food poisoning by algae (This cost includes societal cost, cost to the individual and different affected parties) Todd (1995)$787.5 K Cost per case of death
$1,951 Cost per case of reported illness Hoagland et al. (2002)$1,533 Cost per case of unreported illness
$1.4M Cost per case of death$207/km Cost per kilometer of coastline for the European Union Hoagland & Scatasta (2006)
$2,281/km Cost per kilometer of coastline for the United States$572–$586–$664 Min. cost – Avg. – Max. for a case of respiratory illness Hoagland et al. (2009)
$1,025–$2,160 Low and high cost per emergency department visit for RI and DI Hilborn et al. (2014)
$4,670–$15,620 Low and high cost per inpatient admission for RI and DI
$166 Daily cost of absenteeism per case of illness (cost-of-illness treatment and loss of productivity) Nierenberg et al. (2010)$253.7 Cost of presenteeism (WTP per beachgoer to have an additional lifeguard during the bloom period)
$64 Cost per case of gastroenteritis due to direct contact with water Ralston et al. (2011)$130 Cost per case of illness due to food poisoning
$5.3M Cost per case of death$1,613 For each reported case Morin et al. (2016)
$749 For each unreported case$1,146 Mean cost for each case (reported or unreported)
$1,464 For each reported case Rongo & van Woesik (2012)$423 For each unreported case

Costs in 2016 (US dollars).

K, Thousand; M, Million; DI, Digestive illness; RI, Respiratory illness.

Symptoms are related to the type of contact with contaminated water. Among non-food contacts, swimming appeared as the riskiest, with the greatest number of symptoms of all types. Skin symptoms were most frequently cited in the studies. Some cases of death were reported in the literature (Jochimsen et al. 1998; Carmichael et al. 2001; Azevedo et al. 2002). In fact, in Brazil about 50 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 2009).

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 foods exposed to toxins, for most crustaceans, mollusks, and fish (Todd 1995; Andreatta et al. 2012; Sanseverino et al. 2016). Several other categories of food poisoning are therefore listed under different names, for example, amnesia shellfish poisoning (ASP), paralytic shellfish poisoning (PSP), diarrhea shellfish poisoning (DSP), neurotoxic shellfish poisoning (NSP), Azaspiracids shellfish poisoning (AZP), and ciguatera (ciguatera poisoning). A study in Canada (Todd 1995) calculated an annual estimate of 150 cases of PSP, 50 cases of DSP, and 325 cases of ciguatera. These cases were determined based on a combination of official data (Health and Welfare Canada) and hypotheses established by experts (Todd 1976, 1989a, 1989b, 1989c, 1992).

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 (Lopez et al. 2008; Bláha et al. 2009; Cheung et al. 2013). These chronic effects are, however, ‘more difficult to highlight than acute effects’ (Belleville et al. 2009).

#### Reported cases of health episodes

Among the health episodes, the study of Hilborn et al. (2014) reported some health episodes for the years 2009/2010 in the United States following 11 epidemics associated with freshwater and toxic algae (cyanobacteria). Of the 58 persons surveyed, two were hospitalized, 34 consulted with a healthcare provider, and seven visited the emergency department. No death was recorded. A first estimate of the number of cases of the disease following harmful algae contamination was made (Figgatt et al. 2016) over the period 2008–2014 for the state of New York. In this study, the authors found that 228 people visited hospitals over the 5-year period considered. This equals about 32 visits per year. Thereafter, 17 cases of algae contamination for the year 2015 in New York state (Figgatt et al. 2017) were listed. These cases included primary care and emergency visits; no hospitalization was specified. A study (Carmichael & Boyer 2016) identified human and animal disease cases for the Great Lakes region of North America. The authors identified 68 region-wide cases over the 2010–2015 period, an average of 12 cases per year. A Quebec public health report (MSSS 2014) on blue-green algae indicated that from 2006 to 2012, the public health department received 34 reports of diseases potentially related to harmful algae. These reports involved 77 people, but only 25 cases were probably related to harmful algae. An epidemiological study (Lévesque 2009) conducted in Quebec in summer 2009 on a sample of 466 people found that, for example, 69% of participants reported respiratory symptoms, 49% reported headaches, and 58% reported gastrointestinal problems. Following a bloom of algae in Sarasota County, Florida, an annual estimate of visits to emergency services between 2001 and 2006 was conducted (Hoagland et al. 2009). Emergency services for respiratory diseases received an average of 76 visits per year (min = 39; max = 218).

Diseases reported because of contact with water potentially infected with algae are not all directly caused by algae; there are suspected cases (Figgatt et al. 2017). However, some cases are confirmed to be directly caused by toxic algae, including cyanobacteria. These cases of reported diseases are underestimated, according to Todd (1989c), who proposed a multiplier of 10 as a reasonable figure, especially for food contamination cases by toxic algae. According to him, the reported diseases represent only 10% of the total diseases. This multiplier is also used in other studies (Anderson et al. 2000; Hoagland et al. 2002).

### Costs related to the disease

Different methods were used to estimate costs associated with the disease caused by algae (Table 5). Todd (1995) estimated costs associated with marine food poisoning. This study in Canada was based on an estimate per case of disease of $2,268 for PSP,$1,355 for DSP, and $1,605 for ciguatera. Costs were calculated based on several assumptions and price estimates. The author took the following prices:$158 for a visit or treatment with a doctor, the cost of hospitalization at $788/day and$473/night, and intensive care costs at $2,362/day. The study also considered the cost of emergency transportation and laboratory tests as estimated at$315–$630. Moreover, time spent investigating patients with an epidemic disease was estimated at$788. The value of a lost life (death) was $787,511. Starting with the basis that only 10% of diseases were reported (Todd 1989b; Hoagland et al. 2002), Hoagland et al. (2002) found that the cost per case of illness was between$1,951 and $1,533 for unreported diseases. These costs considered the costs of hospitalization and loss of productivity for the sick individual. In addition, this study estimated the cost of one death at$1.4M. Hoagland & Scatasta (2006), in addition to estimating the cost of disease caused by algae, proposed an estimate of the cost of the disease according to the length of coastline available to the countries. With a coastline length of 65,514 km for the European Union and 19,924 km for the United States, the public health cost was $207/km and$2,281/km, respectively. In their study on the costs of respiratory diseases in Sarasota County, Hoagland et al. (2009) estimated the cost of respiratory disease with the hypothesis that the disease lasts 3 days (1 day of treatment and 2 days of recovery). This hypothesis was based on the American and British guidelines for the treatment of moderate asthma diseases (NHLBI 2007; British Thoracic Society 2008). The cost of the disease was the sum of the costs of medical services and loss of productivity during the period of illness. According to the severity of the disease, the authors found costs ranging from $572 to$664, with an average cost of $586 per case of respiratory illness that visited the emergency department. This average cost does not differ from that obtained by Nierenberg et al. (2010) who found a daily cost of illness of$166 per case ($190 per day for Hoagland et al. (2009)). This figure corresponded 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 beachgoers are willing to pay to have one additional lifeguard; this was estimated at$253.7 per beachgoer.

#### 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.

### Overall cost

Having a general insight into potential health costs following exposure to HAB is important because it could help policy planning and decision-making. At the national level, the effect on public health represents the largest share of the impact of algae and is estimated to be about 42% of the total impact (Anderson et al. 2000; Hoagland et al. 2002). Knowing the source and type of contamination could help authorities in planning an effective fight against HABs. Studies have shown that the main source of contamination is drinking water (domestic use) and recreational activities (Hoagland et al. 2009, 2014; Wood 2016). Focusing on animals revealed that dogs and livestock are the most affected by drinking water contamination (Wood 2016).

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, 1 for treatment and 2 for recuperation (Hoagland et al. 2009, 2014; Ralston et al. 2011). We used treatment cost at $50 for mild illness,$500 for moderate, and $10,000 for severe illness (Ralston et al. 2011). We used the same prices for digestive and respiratory illness since we do not have evidence that one treatment is more expensive than the other. For severe disease requiring hospitalization, we used 5 days' hospitalization and 15 days' recuperation (Hoagland et al. 2014). Presenteeism may be estimated to be between 10% and 13% of productivity loss (Nierenberg et al. 2010). We used a daily income of$120 (Hoagland et al. 2009, 2014). For QALYs losses, we combined adults' data from Table 6. Gastroenteritis QALYs' losses are used as a proxy for digestive illness and influenza-like illness as a proxy for respiratory illness. For a mild case, we supposed a zero QALY loss. A loss of life is valued at $3M dollars (Hoagland et al. 2002; Ralston et al. 2011). We did not assume a value for pain and suffering, but it can be approximated by presenteeism as discussed by Nierenberg et al. (2010). Since medical expenses vary depending on countries and residential areas, our costs estimate mainly reflects those in use in Canada and the United States in a societal perspective. Table 6 Potential QALYs lost following exposure to harmful algae Symptoms/illnessQALYs lostReferences Gastroenteritis 2.2 [95% CI: 1.7; 2.7] using HUI2; 7.1 [95% CI: 5.1; 8.5] using VAS; per 1,000 cases of gastroenteritis in children Brisson et al. (2010) (Canada) 1.8 [95% CI: 1.0; 2.7] using HUI2; 3.1 [95% CI: 2.0; 4.1] using VAS; for caregivers per 1,000 cases of gastroenteritis in children 3.1–3.5 per 1,000 children; using HUI2; 7.7–8.7 per 1,000 family units; using EQ-5D-5 L Marlow et al. (2015) (United Kingdom) Visual disturbance or mild impairmenta 8.3 per 1,000 cases in population younger than 40; using published articles' estimates Wittenborn et al. (2013) (United States) Influenza-like illness 7.5 [min–max, median: 0–44, 6] per 1,000 cases of influenza-like illness (adults and children); using EQ-5D van Hoek et al. (2011) (United Kingdom) Angina 149.72 per 1,000 adults; using EQ-5D Ock et al. (2015) (South Korea) Breathing difficulty 0.16 for little difficulty and 0.771 for a great deal of difficulty per child; using paired comparison responses (similar to time trade-off) Craig et al. (2016) (United States) Symptoms/illnessQALYs lostReferences Gastroenteritis 2.2 [95% CI: 1.7; 2.7] using HUI2; 7.1 [95% CI: 5.1; 8.5] using VAS; per 1,000 cases of gastroenteritis in children Brisson et al. (2010) (Canada) 1.8 [95% CI: 1.0; 2.7] using HUI2; 3.1 [95% CI: 2.0; 4.1] using VAS; for caregivers per 1,000 cases of gastroenteritis in children 3.1–3.5 per 1,000 children; using HUI2; 7.7–8.7 per 1,000 family units; using EQ-5D-5 L Marlow et al. (2015) (United Kingdom) Visual disturbance or mild impairmenta 8.3 per 1,000 cases in population younger than 40; using published articles' estimates Wittenborn et al. (2013) (United States) Influenza-like illness 7.5 [min–max, median: 0–44, 6] per 1,000 cases of influenza-like illness (adults and children); using EQ-5D van Hoek et al. (2011) (United Kingdom) Angina 149.72 per 1,000 adults; using EQ-5D Ock et al. (2015) (South Korea) Breathing difficulty 0.16 for little difficulty and 0.771 for a great deal of difficulty per child; using paired comparison responses (similar to time trade-off) Craig et al. (2016) (United States) aAuthors' calculations: we combined population suffering from injury and burns and visual disturbance and assumed that their QALY lost was 5% of the total QALYs lost in the visual impairment category. Table 7 Overall cost by disease and severity CDTotal (A + B + C + D) A TreatmentB Income lossPresenteeism (10% loss of productivity)QALYs lost (1 QALY =$50 K)
Digestive illness Mild 50 3*12 86
Moderate 500 3*120 0.0031 1,015
Severe 10,000 20*120 0.0041 12,605
Respiratory illness Mild 50 3*12 86
Moderate 500 3*120 0.0075 1,235
Severe 10,000 20*120 0.044 14,600
Death      3M
CDTotal (A + B + C + D)
A TreatmentB Income lossPresenteeism (10% loss of productivity)QALYs lost (1 QALY = $50 K) Digestive illness Mild 50 3*12 86 Moderate 500 3*120 0.0031 1,015 Severe 10,000 20*120 0.0041 12,605 Respiratory illness Mild 50 3*12 86 Moderate 500 3*120 0.0075 1,235 Severe 10,000 20*120 0.044 14,600 Death 3M Costs in$2016 (US dollars).

M, Million.

We determined that a moderate case of illness due to contamination by HAB costs around $1,000 and a mild case costs around$100 (Table 7). The major health cost is due to fatal cases, which could be estimated at $3M. Using a small figure of 1,000 people affected each year, with 75% mild cases, 24% moderate, and 1% death, this could lead to a global burden of$30.3M each year.

## 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 bias which may occur in estimating health costs due to harmful algae exposure. Most of the time, ‘surveillance systems record only 1–10% of foodborne cases’ (CDC 1988; Huss et al. 2004) as stated in Ralston et al. (2011). These unreported cases may be because people do not seek medical care since these cases are mild or familiar to local residents, and they know how to deal with it. This idea is supported by another author (Todd 1989c), who supposed that only 10% of illness are reported. To address these unreported illnesses, reported illnesses are often multiplied by 10 (Todd 1995; Hoagland et al. 2002). This rule of multiplying by 10 may be an effective approximation, but it may either underestimate or overestimate the real cases.

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 harmful algae exposure in the absence of a systematic test of patients. This situation can also lead to many cases which may not be recorded because they were not diagnosed as related to harmful algae.

Chronic long-term effects are more difficult to highlight (Belleville et al. 2009). No studies have included costs related to long-term effects of chronic exposure to harmful algae. This insufficiency in reporting long-term effects may be caused either by the misleading symptoms or by an absence of follow-up with people living near a water source or continuously exposed to contaminated water. Some authors (Lopez et al. 2008; Bláha et al. 2009; Cheung et al. 2013) have shown that health problems develop in the long term such as liver cancer, cardiac arrhythmia, or neurodegenerative diseases. Estimating the long-term effects of chronic exposure to harmful algae, especially cyanobacteria, is also difficult in the way that it is difficult to isolate the exact contribution of cyanobacteria in the occurrence of the disease in the long term.

For some premature deaths due to acute exposure, there is no consensus regarding the value to consider, since many authors in this review considered different price setups according to the methodologies (e.g., hedonic wage, willingness to pay, and human capital) and hypotheses used (Todd 1995; Hoagland et al. 2002). However, one can consider the results of meta-analysis in the work of Viscusi & Aldy (2003).

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 al. 2010) discussed it but did not include it, as the authors acknowledge that they cannot estimate these costs, even if the cost of pain and suffering could be included in the calculation of QALYs lost due to harmful algae exposure. Also, since the studies included in this review provided too little information about the different kinds of HABs, it was impossible for us to estimate specific costs by the type of toxins.

There are many other studies which present costs of waterborne illness or foodborne illness that could be interesting to discuss here since they have some similarity to those about harmful algae. For example, some authors (DeFlorio-Barker et al. 2018) estimated the costs related to a set of recreational waterborne illnesses (gastro, respiratory, skin, eye, and ear) in the United States. Using multiple cases of illness severity varying from benign to moderate to severe, the authors found that the costs were, respectively, $11,$270 and $350,370 per case of illness (in$2016). These authors define a benign illness as a case where the sick person did not meet a healthcare provider, while a moderate illness is defined as a situation where the patient received a medical consultation either externally or in emergencies. Severe illnesses are defined as those requiring hospitalization or resulting in death. These estimates were not made in the context of illness due to harmful algae but in the general case of waterborne illness. Since the illness source and symptoms are similar, these costs can easily be extrapolated to our context.

In another study (DeFlorio-Barker et al. 2017) focusing on gastrointestinal illness associated with water recreation in the United States, the authors found that costs of illness were $1,220 (95% CI:$338–1,681) for incidental contact and $1,676 for swimming/wading (95% CI:$425–2,743) per 1,000 recreational water users (in $2007). The authors highlight the fact that loss of productivity accounts for up to 90% of total costs. Furthermore, they found that the cost for marine recreational water users was higher than for freshwater recreational water users. Given et al. (2006) also estimated the public health cost of contaminated coastal water. They estimated between 628 K and 1.5M cases of gastrointestinal illness caused by swimming in contaminated water in California. This figure yields a total cost varying from$21M to $51M (in$2000). Dwight et al. (2005) found the same cost as Given and colleagues in estimating the economic burden of illness associated with recreational coastal water pollution in California. These last authors found a cost (in $2001) of$36.58 per gastrointestinal illness and $76.76 per acute respiratory disease. The costs for earache and eye ache were, respectively,$37.86 and $27.31. Even if these costs may be far from those used in Table 6, the authors cited some studies (Liddle et al. 1997; Carabin et al. 1999) which found the same costs as in Table 6. All of these costs estimated to access the economic impact of HABs on human health should be considered when evaluating the monetary benefits of improving water quality (DeFlorio-Barker et al. 2017). In this area, Hunter et al. (2012) evaluated the WTP of the public to reduce health risks posed by toxic algal blooms in Scotland (United Kingdom). With 55% of respondents willing to pay to reduce health risks, the authors found a WTP between$16.93 and 20.73 per household and per year. An aggregation of this amount over a small city of 10,000 households could lead to a total benefit of $170 K per year. Nunes & van den Bergh (2004) also tried to estimate the value people give for protection against invasive marine species in the Netherlands. Using a combination of travel costs and contingent valuation methods, the authors found that the benefits per individual were, respectively,$83 and \$115. The survey also revealed that ‘respondents with relatively high travel costs have a relatively low WTP for the marine-protection program.’ Evaluating the cost of water treatment benefits could also be difficult since it could be confusing to separate the cost of routine water treatment from those due to pollution by HABs (Dodds et al. 2009).

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 (1995) concerned sporadic events across Canada; this is the case for Hoagland et al. (2002). 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. 2008).

Finally, the fact that some studies used survey and self-reported 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.

## ACKNOWLEDGEMENTS

This study was funded by Genome Canada. 2015 Large-Scale Applied Research Project Competition: Natural Resources and the Environment: Sector Challenges – Genomic Solutions.

None to declare.

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