Swimming in Stinging Water: A Case Report of Acute Response to Rhizostoma pulmo Presence Associated with Microscopic Observation of Free Nematocysts in Mucous Secretions

Abstract

The barrel jellyfish (Rhizostoma pulmo), like other cnidarians, shows cnidocytes containing cnidae, responsible for the jellyfish’s stinging properties. The sting of R. pulmo can cause contact dermatitis or urticaria and even systemic symptoms. Recent studies have identified stinging-cell structures in the mucous secretion released in the water column by Cassiopea xamachana, belonging to the same order as R. pulmo. The present paper verifies the release of stinging-cell structures in the water by R. pulmo and reports the case of two 17-year-old adolescents (one male and one female) who were affected by epidermal rashes consistent with the irritating sensations of stinging water. The reaction happened twice in the Ionian Sea; the patients were in proximity to R. pulmo but, on both occasions, there had been absolutely no direct contact with the jellyfish’s tentacles. To test the hypothesis of stinging water caused by R. pulmo, samples of sea water and mucous harvested in close proximity to a living jellyfish were taken and analyzed under a microscope at different magnifications. The microscopic analysis showed the presence of free and aggregated nematocysts in both the samples of water and mucous. It is likely that the free and aggregated nematocysts observed were discharged in the water by the jellyfish and were dispersed by water currents that led them to come into contact with the patients’ skin. At present, it is not known what predisposes humans to the perception of stinging water, and it is reasonable to affirm that caution should be advised for people with an allergic history when entering the water in the presence of jellyfish. Further investigations are required to better understand both the pathophysiological pathways underlying the stinging water phenomenon and the minimum concentration of urticating elements that is able to trigger the onset of stinging water.

1. Introduction

The body of cnidarians. The body of cnidarians is mainly composed of three cellular layers: an inner layer of epithelium called the gastrodermis, which lines the inner cavity; a medial mesoglea, a gelatinous layer of connective tissue; and an outer epidermis that is exposed to the external environment, covering both the umbrella and tentacles [1]. Most of the cells within a jellyfish’s body are either in the epidermis or the gastrodermis; among them, there is a cytotype that is a defining feature of cnidarians, the cnidocyte [1]. Each cnidocyte contains a cnida, a membranous capsule filled with fluid that derives from the Golgi apparatus and that encloses an eversible tubule, and a cnidocil, a mechanoreceptive sensory cilium that triggers the cnida discharge [1,2]. Cnidae can be subdivided into three groups: nematocysts, shared by all cnidarian species, with spines or barbs on the eversible tubule that are responsible for the jellyfish’s stinging properties; spirocysts, thin-walled cnidae typical of anthozoans that lack cnidocils and have adhesive microscopic threads radiating from the eversible tubule that is coiled inside the cnida; and ptychocysts, which occur only on the epidermis of anthozoan tube anemones (subclass Ceriantharia Perrier, 1893), and resemble spirocysts but differ in the folding of the eversible tube [1,2].

Rhizostoma pulmo. The barrel jellyfish (Rhizostoma pulmo Macri, 1778) is one of the largest scyphomedusae from the family Rhizostomatidae which is endemic to the Mediterranean Sea. Adults in the medusa stage can reach very considerable sizes ranging from 15 up to 60 cm [3,4,5]. This adult stage is characterized by a blueish-colored semispherical and dome-shaped umbrella, with eight fleshy oral arms and an umbrella edge that is tentacle-less [6]. R. pulmo is widely distributed throughout the Mediterranean basin and blooms have been frequently reported [5,6,7,8], although its presence is also well documented in the Eastern Atlantic Ocean and in the Black Sea [5]. Sightings of R. pulmo blooms are increasing [9,10], and even if they could be caused by coastal eutrophication [5], they are difficult to predict [10]. Lilley et al. [4] argued that this tendency was already present during the late 20th century, and swarms of R. pulmo have been regularly documented from 2005 onward in the Ionian Sea every year from April to December, with peaks ranging from July to October [6]. The possibility that their blooms may impact marine biodiversity and coastal communities in general has also been discussed [6,10,11,12,13,14]. Along with the ecological effects, the socio-economic effects also need to be taken into account; in fact, jellyfish blooms can impact touristic activities due to beach closures and human stings [15]. Despite the fact most people consider R. pulmo as a harmless species, Avian et al. [16] identified as many as four different kinds of nematocysts (heterotrichous microbasic euryteles, holotrichous isorhizas, atrichous a-isorhizas, and atrichous-isorhizas) in R. pulmo’s tentacles and umbrella.

Health problem for humans and mucous secretion. Kokelj and Plotzer [3] reported four cases of contact dermatitis caused by R. pulmo stings, confirming its toxicity to humans: the contact was reported to cause immediate cutaneous pain, followed by erythematous, slightly infiltrated eruption and formation of vesicles; after local corticosteroid therapy, the pain disappeared within 36 h. Before them, several other authors reported further reactions caused by contact with R. pulmo: burning on the skin and particularly the lips, sneezing and rhinorrhea after handling dried specimens, and urticaria and systemic symptoms after stings [3]. The possibility of shedding body fragments, active propagules, or even just DNA in water has been widely described for many life forms [17]; notably, Ames et al. [18] identified particular stinging-cell structures in the mucous secretion released in the water column by a benthic upside-down jellyfish (Cassiopea xamachana Bigelow, 1892) belonging to the same order as R. pulmo, Rhizostomeae (Cuvier, 1799). This stinging structure discharge is particularly known among snorkelers, who describe the phenomenon as stinging water. Even R. pulmo is able to produce mucous secretions [6], probably as a defense mechanism or from natural tissue autolysis [19]. Several studies have given insights into the role of external stressors like sediment concentration, air exposure, UV irradiation, and mechanical stimuli, which can be promoting factors for mucus production [6,19,20,21,22,23,24]. Furthermore, as reported by Bythell and Wild [25], mucus discharge could also be triggered by ocean acidification and global warming.

This case report describes a case of possible stinging water in two adolescents caused by exposure to free nematocysts released by R. pulmo. For the first time, stinging elements from R. pulmo were detected in mucous secretions and in the water around a living jellyfish, suggesting a possible explanation for the clinical presentations observed in the patients. While symptoms are mild, caution should be advised for individuals with a prior history of allergies due to possible cross-reactivities with jellyfish stinging structures.

2. Case Presentation

Patients. In August 2023, along the Gulf of Taranto, two 17-year-old adolescents (one male and one female) reported epidermal rashes consistent with the irritating sensations of stinging water. Both of the patients are of Caucasian ethnicity and Italian nationality and both are highly familiar with swimming in sea and pool water. The male patient presented no active allergies but a history of allergies to dust mites of the genus Dermatophagoides in pediatric age. The female patient suffers from an active allergy to alimentary colors, in particular to cochineal red (E120) and Blu Patent V (E131).

Stinging water. On the first day, the patients were swimming in deep water alongside some Rhizostoma pulmo individuals without directly touching their bodies or tentacle fragments. After 20 min of swimming, a general sense of discomfort all over the submerged skin was reported by both patients; the female also reported skin irritation consistent with a jellyfish sting spreading all over the shoulders and upper thorax with accentuation on the sternum area, whereas no itching or urtication was reported by the male patient. The day after, the same painful sensation was described by both patients on the submerged leg skin while walking for half an hour in shallow calm water (20/30 cm deep) on the shoreline. No jellyfish was sighted near the patients on the second day; considering the size of jellyfish and water transparency, an involuntary direct contact is to be excluded. In both cases, the painful sensation was significantly lowered by coming out of the water and was completely eliminated upon showering.

Water analysis. To test the hypothesis of stinging water caused by Rhizostoma pulmo, samples of sea water and mucous in close proximity to a jellyfish were taken on the third day, stored in zip-lock bags, and immediately preserved at −20 °C [16]. Once in the lab, the water was left at room temperature for two hours and allowed to thaw completely. Water samples were randomly taken with disposable Pasteur pipettes and smeared over microscope slides. Brightfield microscopic observations were carried out at 20×, 40×, and 100× magnifications with a Zeiss Standard 25 microscope (Oberkochen, Germany) and acquired with a T-EsseLab True Chrome HD II S microscope camera (Milano, Italy).

The microscopic observation carried out in this work allowed the observation of both nematocyst aggregates (Figure 1A), similar to those that can be found on the epidermal surface of tentacles, and of free nematocysts, both undischarged (Figure 1B) and discharged (Figure 1C,D).

3. Discussion

This work reports two independent cases of skin irritation most likely caused by the indirect action of free jellyfish nematocysts. The two subjects reported pain similar to that of a jellyfish sting upon coming into contact with the tentacles, but spread all across large portions of the body that were submerged. Aquagenic urticaria was excluded due to the patients’ histories. It is probable that, as reported for Cassiopea xamachana [18], the free and aggregated nematocysts observed were discharged in the water by the jellyfish and were dispersed by water currents that led them to come into contact with the patients’ skin. Even though the nematocyst type could not be precisely determined based solely on light microscopy observations, the capsule morphologies observed are consistent with heterotrichous microbasic euryteles (Figure 1A–C) and heterotrichous isorhizas (Figure 1D), as described by Avian et al. [16]. Nevertheless, all nematocyst types still retain the capability of injecting toxin [2]. The patterns of irritation and the pain manifestation suggest that these stinging elements are more abundant on the surface of the water than in the rest of the water column. Furthermore, there is reason to believe that the phenomenon could be exacerbated by some environmental factors that promote jellyfish mucus secretion, as described in the Introduction.

Generally, contact with nematocysts causes an effect similar to a prick due to the mechanical penetration of the thread into the tissues, and the activity of mast cells. The injected substances irritate the nerve endings and cause the characteristic stiffness, swelling, itchiness, and pain [26]. Even though the venom of cnidarians differs among species, it is mainly composed of proteins, peptides, and other substances of pharmacological concern [27]; as reported by Turk [28], peptidic sodium channel neurotoxins, cytolytic proteins, and non-peptidic toxins have been discovered in cnidarians. All these toxic substances can act on humans as antigens, therefore evoking a defense response by the immune system with consequent production of specific antibodies and activation of the “memory” phenomenon. This event is particularly evident in the case report by Imamura et al. [29], in which the ingestion of a jellyfish in a patient previously sensitized through skin stings caused an anaphylactic reaction. Furthermore, an even more interesting case, especially in relation to the event here described, is reported by Okubo et al. [30], describing a case of anaphylaxis after jellyfish ingestion without any history of jellyfish contact or stings. The patient, a 14-year-old boy, developed a cough, urticaria, and dyspnea 30 min after a breakfast meal that included dried and salted jellyfish. The patient had never been to the sea and had no previous episodes of jellyfish contact or stings. Even more interestingly, the patient from Okubo et al. [30] had no past medical history other than a house dust mite allergy, just like one of our patients. Because a specific IgE antibody test for jellyfish was unavailable, a prick-to-prick test for dried and salted jellyfish was performed, and it resulted in a positive skin reaction as strong as a positive reaction produced by house dust mites. To date, however, no antigens are known that can cause a cross-reaction between the proteins of jellyfish and house dust mites, but, as already happens between the latter and crustaceans via tropomyosins, this hypothesis cannot be completely excluded, and further research should be carried out to identify new reliable biomarkers to assess the immune responses to allergies [31]. Another clinical case that could be attributable to stinging water, although not explicitly discussed by the authors, was reported by Quarantiello et al. [32], describing the case of an 8-year-old female who presented a widespread urticarial rash after swimming in the sea. It was treated with 3% aluminum chloride gel, oral antihistamine and cortisone, as with any injury from a jellyfish sting, even though the little girl did not show any immediate subjective symptoms while she was in the water, as if she had not felt contact with the jellyfish while bathing. It is not currently known what predisposes humans to the perception of stinging water, and despite the fact the cases reported did not require either systemic or local therapy, it is reasonable to affirm that, as a preventative measure, maximum caution is recommended for people with an allergic history. Further investigations are required to better understand the pathophysiological pathways underlying the stinging water phenomenon.

4. Future Perspectives

To date, it has not been possible to determine a quantitative parameter such as the minimal critical concentration of jellyfish stinging elements in the water able to cause the stinging water phenomenon that can be responsible for skin reactions. The hardship in quantifying this phenomenon is to be found in the fact that, firstly, the stinging structures are diluted in the vast marine environment, with their concentration varying according to wind, sea conditions, and proximity to jellyfish. Secondly, the skin reaction appears to be significantly influenced by individual predisposition and thus depends on each person’s sensitivity. Future studies, stemming from this preliminary finding, but specifically aimed at quantifying these parameters, would be of great interest, especially looking into the possibility of stinging water caused by more venomous species.