# Case Report: Two Cases of Keratoconjunctivitis Tied to *Sargassum* Algae Emanations

Harold Merle,¹* Dabor Resière,² Charles Mesnard,¹ Mitta Pierre,¹ Albert Jean-Charles,¹ Laurence Béral,³ and Rémi Nevière⁴

¹Department of Ophthalmology, University Hospital of Martinique, Fort de France, France (French West Indies); ²Critical Care Unit, University Hospital of Martinique, Fort de France, France (French West Indies); ³Department of Ophthalmology, University Hospital of Guadeloupe, Pointe à Pitre, Guadeloupe; ⁴Department of Cardiology, University Hospital of Martinique, Fort de France, France (French West Indies)

**Abstract.** Since 2011, considerable amounts of *Sargassum* algae regularly end up on beaches in the Gulf of Mexico, the Caribbean, and in the French overseas departments. We report observations of two bilateral keratoconjunctivitis associated with important functional symptomatology. There was a conjunctival hyperemia and superficial punctate keratitis. The ocular impairment would repeat at every algae ashore landing. Clinical examination, history, and time line of symptomatology onset allowed us to eliminate the classic etiologies of bilateral keratoconjunctivitis and to suggest an irritant toxic origin tied to hydrogen sulfide. This is the first description of ocular impairment tied to *Sargassum* algae decomposition. Their decomposition, through H₂S emission, can be at the origin of bilateral keratoconjunctivitis. Ocular impairment is often at the forefront of complaints made by individuals exposed to H₂S.

## INTRODUCTION

The Gulf of Mexico, the Caribbean, and in particular the French overseas departments have been facing massive and recurring waves of *Sargassum* algae washing ashore since 2011.¹⁻³ The layer can be several meters thick, and the floating clusters can cover entire bay areas. In Martinique, the total washed-up biomass is estimated to be 58,000 tons. Contrary to what was originally believed, the algae are not from the Sargasso Sea but would most likely be from a new growth and accumulation zone located north of Brazil, a consequence of climate factors as well as increasing deforestation of Amanzonia.⁴ Removing the algae is very difficult, and they decompose on site. Their decomposition comes with highly elevated hydrogen sulfide (H₂S) emissions in the ambient air.² Hydrogen sulfide is one of the most dangerous gases. Hydrogen sulfide is corrosive, explosive, and flammable.⁵ Between January 2018 and August 2018, more than 8,000 people went to see their general practitioners, and many schools were closed for several months in Martinique because of the impairment felt by the population exposed to H₂S. Among the people seeking medical consultations, about 50% described ocular irritation symptoms. The other signs were sneezing, runny nose, headache, insomnia, nausea, and difficulty breathing.⁶ We report the first observations of keratoconjunctivitis linked to H₂S toxicity from algae decomposition.

## CASE REPORT

A 58-year-old woman and a 59-year-old man presented themselves for a consultation at the University Hospital of Martinique to renew their optic correction as well as for a bilateral ocular redness that appeared 8 days earlier. They had no medical preconditions nor were they under medical treatments. They lived in a city on the south side of Martinique where *Sargassum* algae regularly landed ashore. Their house was located about 50 m from the beach, on which about 10 days ago, a significant quantity of algae had landed (Figure 1).

**Case 1.** Mrs M did not show visual acuity decrease but complained of a grain of sand sensation, of a foreign body, itching, and intermittent eye watering. Her visual acuity in both the eyes was 20/20, with the right glasses correction. The bulbar and palpebral conjunctiva showed signs of diffuse hyperemia without follicle, papilla, chemosis, limestonecretion, membrane, or hemorrhage (Figure 2). There were on both the eyes about 10 punctate erosions of the corneal epithelium, soaked by fluorescein and located in the inferior part of the eyelids' opening area (Figure 3). The overall cornea was clear; there was no stroma edema, opacities, or corneal neovessels. The anterior chamber was not inflammatory. Ocular tonus and funduscopy were normal.

**Case 2.** Mr M had a visual acuity of 20/20 with glasses correction. He also complained of the grain of sand sensation and itching in both the eyes. There was a bilateral diffuse conjunctival hyperemia, without any other impairment on the conjunctive. The right eye's cornea had keratitis with less than 10 puncture epithelial erosions colored by fluorescein. Examination of the left eye's cornea was normal. The rest of the ocular examination was normal.

In both cases, eyelid examination and ocular motility were normal, and there were no preauricular adenopathy. There were no secretions, or scabs in the eyelashes, nor cornea hypoesthesia. Schirmer 1 test and break-up time were normal. This ocular symptomatology was isolated and was not accompanied by otorhinolaryngological or bronchial signs. The treatment put in place was lubricants without preservatives and applied at least six times per day in both eyes. It significantly reduced the functional signs without reducing the hyperemia. The bilateral keratoconjunctivitis appeared 48 hours after the algae washed ashore and was present during the whole decomposition time of the algae, which the patients could pinpoint because of the typical rotten egg smell of H₂S. Functional signs and ocular redness disappeared about 48 hours after the end of noticeable H₂S smell. Questioning allowed us to find similar ocular irritation episodes which occurred every time there were massive amounts of algae washing ashore.

## DISCUSSION

This is the first description of ocular impairment tied to *Sargassum* algae decomposition. Superficial punctate

<footnote>*Address correspondence to Harold Merle, Department of Ophthalmology, University Hospital of Martinique, Hôpital Pierre Zobda Quitman, BP 632, 97261 Fort de France Cedex, Martinique - France (French West Indies). E-mail: harold.merle@chu-martinique.fr</footnote>
<figure><img src="image_1.png" /><figcaption>FIGURE 1. *Sargassum* on a beach in Martinique.</figcaption></figure>

keratitis and conjunctivitis are nonspecific lesions on the oc-ular surface that occur because of aggressions of a variety of toxins. Clinical examination, history, and onset time line of the symptomatology allowed us to eliminate classic etiologies of bilateral and synchronal keratoconjunctivitis (infectious, in-flammatory, iatrogenic, mechanic, and allergic) and to suggest the toxic irritant origin linked to H₂S. Short onset time present during H₂S smell perception is in favor of direct and imme-diate toxic effects on the ocular surface capable of inducing a rapid inflammatory reaction.

Sargassum algae that wash ashore in the Caribbean belong to two different species: *Sargassum natans* and *Sargassum fluitans*. They are brown or yellow macroalgae without cram-pons that would allow them to attach to a substrate. They have lateral ramified and tangled branches, on which many floaters are located, and gas bladders.² No organic component of the fresh algae poses a health threat. When the algae are not regularly picked up, they amass, and, on the top, a scab layer forms, which prevents oxygen diffusion. During anaerobia decomposition, the sulfur present in the *Sargassum* leads to H₂S production. Hydrogen sulfide is a colorless gas, heavier than air, which has a characteristic smell of rotten eggs. Ef-fects of acute exposure to H₂S on human with concentrations superior to 50 ppm (parts per million) are well known, of in-creasing gravity with concentration, and can lead to death (Table 1).⁵ They are less documented for sub-chronic and chronic exposures (≤ 10 ppm).⁷ Studies of population living next to industrial sites which emit H₂S (paper factories, natural gas production, and intensive livestock farming) have shown the increase of nasal irritation, and respiratory and ocular symptoms.⁸⁻¹⁰

A few references describe the ocular impairment; as early as 1944, Larsen described keratitis among sewage workers ex-posed to H₂S. Besides the classical functional symptomology

<figure><img src="image_2.png" /><figcaption>FIGURE 2. Case 1: bilateral keratoconjunctivitis. Important: bilateral and diffuse conjunctival hyperemia.</figcaption></figure>

<figure><img src="image_3.png" /><figcaption>FIGURE 3. Case 1: right eye. Keratitis with less than 10 puncture epithelial erosions colored by fluorescein and located in the inferior part of the eyelids' opening area.</figcaption></figure>

associated with exposure (disappearing when the workers would get back to the surface), corneal lesions manifested through superficial punctate keratitis holding fluorescein and located in the opening area of the eyelids.¹¹ Beasley reports three observations tied to H₂S exposure over 4 weeks after an accidental pipe burst. Victims had conjunctivitis associated with keratitis. They complained of ocular pain, photophobia, halo perception, and blurry and cloudy vision. The most severe case also had blepharospasm, severe and bilateral keratitis, as well as important conjunctival inflammation. Ocular signs

<caption>TABLE 1</caption>

Clinical signs of acute hydrogen sulfide intoxication as a function of concentration

<table><thead><tr><th>Concentration (parts per million)</th><th>Clinical signs</th></tr></thead><tbody><tr><td>0.00011–0.00033</td><td>Normal concentration in the ambient air</td></tr><tr><td>0.0005</td><td>Smallest concentration detectable by the olfactory system</td></tr><tr><td>0.01–1.5</td><td>Perception of the rotten egg smell</td></tr><tr><td>2–5</td><td>Watering, headache, insomnia, nausea, breathing, and difficulties in asthmatic patients</td></tr><tr><td>20</td><td>Irritability, tiredness, memory problems, dizziness, and decreased appetite</td></tr><tr><td>50–100</td><td>Irritation of the ocular mucosa, upper airway, and respiratory and digestive tracts</td></tr><tr><td>100</td><td>Conjunctivitis, keratitis, hyposmia, cough, respiratory difficulty, and drowsiness. Death after 48 hours of exposure</td></tr><tr><td>100–150</td><td>Anosmia</td></tr><tr><td>200–300</td><td>Eye damage and respiratory problems (pulmonary edema) after 1 hour of exposure. Disorientation, severe asthenia, and nystagmus</td></tr><tr><td>500–700</td><td>Collapse, loss of consciousness. Death in 30 minutes</td></tr><tr><td>700–1,000</td><td>Death in minutes</td></tr><tr><td>> 1,000</td><td>Death in seconds</td></tr></tbody></table>
were significantly less important on the remaining days and disappeared 48 hours after the end of exposure.¹² In a sheep intestine sausage factory, Luck and Kaye¹³ describe six cases of isolated ocular impairment. They were bilateral keratoconjunctivitis tied to the H₂S produced by putrefaction. Functional symptomatology consisted of blepharospasm, watering, and photophobia. The cornea showed multiple punctiform erosions and the conjunctiva, an important hyperemia. All the signs disappeared about 24 hours after the patients stopped working. Schinasi et al.¹⁴ showed within a population living next to porcine industry that the smell and atmospheric H₂S concentration were linked to the apparition of ocular and respiratory symptoms. There was also observation of increased frequency of cataracts.⁹ Among animals, inhalation of small concentration of H₂S lead to inflammation of the nasal mucous membrane and loss of olfactory neurons.¹⁵ Chronic exposure to H₂S also comes with neurobehavioral (headaches, vertigo, and memory loss) and cardiologic signs.¹⁶

## CONCLUSION

Sargassum algae decomposition represents not only an environmental and economic disaster but also a serious health threat. In more than half of the cases, ocular impairment is at the forefront of symptoms. It involves bilateral keratoconjunctivitis associated with variable functional symptomatology. Long-term impact on visual function is unknown. These observations justify the implementation of first preventative measures by informing the population of sanitary risks linked to H₂S exposition, and also of prospective studies with the objective to define the effects of chronic exposure to lower H₂S dose.

Received June 10, 2020. Accepted for publication June 30, 2020.

Published online December 7, 2020.

Disclosure: All authors attest they meet the current ICMJE criteria for authorship. Consent to publish the case reports were obtained. This report does not contain any personal information that could lead to the identification of the patients.

Authors' addresses: Harold Merle, Charles Mesnard, Mitta Pierre, and Albert Jean-Charles, Department of Ophthalmology, University Hospital of Martinique, Fort de France, France (French West Indies), E-mails: harold.merle@wanadoo.fr, charles.mesnard@chu-fortdefrance.fr, mitta.pierre@chu-fortdefrance.fr, and albert.jean-charles@chu-fortdefrance.fr. Dabor Resière, Critical Care Unit, University Hospital of Martinique, Fort de France, France (French West Indies), E-mail: dabor.resiere@chu-fortdefrance.fr. Laurence Béral, CHU Fort de France, Fort de

France, France (French West Indies), E-mail: laurence.beral@chu-fortdefrance.fr. Rémi Nevière, Department of Cardiology, University Hospital of Martinique, Fort de France, France (French West Indies), E-mail: remi.neviere@chu-fortdefrance.fr.

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