Sensitization and allergy to pineapple and coconut juice in patients followed up for allergic diseases in Parakou, Benin

INTRODUCTION

With globalization and changes in lifestyles and culinary habits, there is an increase in the number of adverse reactions that may occur following food ingestion.^[1] These reactions are a major public health concern, affecting hundreds of millions of people globally and altering considerably their quality of life, as they often lead to dietary avoidance and nutritional deficiencies.^[1] Up to 15–20% of the global population is estimated to suffer from these conditions, which may involve several systems, including mucocutaneous, cardiovascular, respiratory, digestive, and central nervous systems.^[2] Some of the reactions can even be life-threatening, with the development of anaphylaxis.^[3] Several mechanisms, such as immunological, including food allergy or non-immunological toxic, pharmacologic, and metabolic reactions, may lead to these conditions.^[4]

Despite the pejorative consequences cited above, these diseases remain poorly studied in low- and middle-income countries, in contrast to more developed settings, where most of the studies have been carried out and focused on foods found in those settings.^[5]

Pineapple (Ananas comosus) and coconut (Cocos nucifera) are two main tropical fruits that are largely consumed in subSaharan Africa. Pineapple is the third most commercialized tropical fruit in the world, after bananas and mangoes, with a growing demand.^[6,7] This sweet fruit has numerous nutrients offering many health benefits,^[7] with its main component, the bromelain, being attributed several virtues, including anti-inflammatory, fibrinolytic, anti-platelet aggregation, anti-edema, anti-cancer, and digestive properties.^[6-8] As for coconut, this smooth fruit is also well appreciated, with a unique chemical composition of minerals, amino acids, sugars, vitamins, and phytohormones.^[9,10]

In our routine practice, patients most often cite both fruits as the cause of adverse reactions during medical consultations in our setting. An allergic mechanism is usually suspected by patients or some practitioners, leading to their systematic avoidance. However, the foods may induce other types of reactions, such as mucosal irritation or intolerance. The present study was initiated to investigate to what extent cutaneous sensitization to both fruits, synonymous with allergy, was present among those followed up for allergic diseases in our setting.

MATERIALS AND METHODS

RESULTS

DISCUSSION

This study complements the few reports in the literature investigating cutaneous sensitization and adverse reactions with tropical fruits in sub-Saharan Africa.

Overall, reports of clinical manifestations after pineapple ingestion were quite common among allergic patients followed in the center, being reported by about half of the patients who were followed up. As for the clinical manifestations, like other studies in the literature, ^[15,16] mouth and lip pruritus were the most reported in nearly four out of ten patients. Interestingly, after having performed SPT with pineapple juice, sensitization was observed in one-third of patients. When considering the clinical history, an allergy to pineapple was diagnosed in almost a quarter of the patients or almost half of those who were symptomatic.

The proportion of patients allergic to pineapple was quite high, confirming local community perceptions that pineapple is a food commonly implicated in allergic reactions. Cases of sensitization and allergy to pineapple have also been reported in the literature from elsewhere. In one study from Ghana, pineapple was the second most commonly reported food with adverse reactions after beans, and it was one of two foods, along with peanuts, to which sensitization was most common.^[17] In another study from Mexico, 8.9% of patients had an oral allergy syndrome, of whom 62.5% were sensitized to pineapple, the main causative food found in the survey.^[16] In a nationwide survey in Korea, 41.7% of 648 hay fever patients had pollen-food allergy syndrome, of whom the causative food was pineapple in 13.7% of cases.^[18] In another report from Denmark, among 16.7% of young adults with pollen-food syndrome, pineapple was the third most commonly reported food after kiwi fruit and hazelnuts.^[19] Reindl et al. demonstrated immediate reactions after pineapple juice consumption in 5% of those suffering from the pollen-food syndrome in their study population.^[20] A number of sensitizations to pineapple have also been reported by Camero-Martínez et al. in Spain among patients who were treated for allergies.^[21]

Due to limited technical resources, we were not able to carry out recombinant testing. However, based on previous literature, two main allergens responsible for allergic reactions to pineapple have been identified: Ana c 1 and Ana c 2.^[22,23] Ana c 1 is a pan-allergen profilin that mainly causes food-pollen allergic syndromes and is responsible for numerous cross-reactivities with pollens such as birch and phleum, with latex, and with many other fruits such as papaya, avocado, banana, passion fruit, melon, mango, kiwi, peach, tomato, and chestnut.^[20,24] Sensitization to this profiling protein, which is degradable by heat and digestive enzymes, mostly occurs through inhalation, and clinical features are often non-severe. In contrast, Ana c 2, a major allergen contained in Bromelain, which is more thermostable, may induce severe reactions such as anaphylaxis.^[23]

With respect to clinical features, along with mouth and lip pruritus, bronchospasm, allergic rhinitis, and conjunctivitis were significantly associated with pineapple allergy diagnosis. Very few patients complained of anaphylaxis-like symptoms, contrary to what has been reported from other studies. ^[3,20] For instance, in a systematic review of 358 cases of anaphylaxis reported in China between 1980 and 2007, pineapple was the most frequently incriminated food, accounting for 25% of cases.^[3]

In contrast to pineapple, complaints of adverse reactions from coconut and coconut-induced cutaneous sensitization were found less frequently. Approximately one person in five complained of clinical manifestations, mostly asthma-like symptoms, and was found to be sensitized to coconut; an allergy to this fruit was confirmed in one-third of those who reported clinical features. In the literature, there are few reports on coconut allergy, but sometimes severe reactions do occur. Thus, Kim and Hussain reported a 2% prevalence of allergy to coconut among patients who were diagnosed with an allergy to latex.^[25] Nine cases of anaphylaxis and 26 other cases with less severe immunoglobulin E (IgE)-mediated allergy to coconut were reported by Pathmanandavel et al. in 2020 from Australia in a pediatric population.^[26] Severe reactions were reported in a 6-year-old child and a 64-year-old woman, respectively.^[27,28] Allergic reactions with this fruit are mainly attributed to sensitization to coc n 1, a protein in the vicilin family.^[29,30]

Elsewhere, several patients complained of symptoms, but the SPT results were negative. These patients represent nearly one-third and one-half of those who reported symptoms after ingestion of pineapple juice and coconut water, respectively. Some of these patients may include those who are allergic but whose diagnosis would have required a specific IgE antibody dosage to be confirmed, but this was not possible in our study due to the unavailability of the reagents in our setting, along with other resource constraints. In addition, this group of patients may include those who are simply intolerant to these fruits.

From a practical point of view, clarifying the mechanism(s) underlining the adverse reactions triggered by the fruit would be helpful to improve patient management and quality of life. For instance, a mucosal irritation triggered by pineapple may allow continued ingestion of the fruit taken with dairy products or with salt; intolerant patients might be able to consume small quantities; those experiencing non-severe allergic reactions might benefit from heating pineapple before eating, while anaphylaxis would require avoidance and epinephrine prescription. ^[3,31,32]

A strength of this study was the use of a native food for conducting SPT and this has been shown previously to have a higher sensitivity and a better negative predictive value compared with commercial extracts.^[33] One limitation, however, was the absence of oral challenge testing, mainly because patients were reluctant to undertake this, with the possibility of an anaphylactic reaction occurring during the test. However, a compatible clinical history combined with a positive SPT result is well-validated for the diagnosis of allergy.^[13]

Finally, there is a need to improve the diagnosis and management of allergic diseases in sub-Saharan Africa, which is experiencing a rapid epidemiological transition. Likewise, we call for more research on these conditions to find out any particularities in this region. This may include, for instance, the investigation of environmental factors contributing to food allergies in sub-Saharan Africa.

CONCLUSION

Among patients who were followed up in Borgou Teaching Hospital, pineapple is a common cause of sensitization and allergy, diagnosed in approximately one-quarter of patients. In contrast, coconuts are less frequently responsible for sensitization and allergy, diagnosed in one in fifteen patients. More studies are required to improve knowledge of allergic diseases in sub-Saharan Africa.