Western Lifestyle and Increased Prevalence of Atopic Diseases: An Example from a Small Papua New Guinean Island
© World Allergy Organization; licensee BioMed Central Ltd. 2009
Published: 15 July 2009
Allergic diseases represent an increasing problem in public health in most modern societies as their prevalence has risen markedly during recent decades. Nevertheless, the causes of this increase are not yet fully explained.
We investigated the correlation of Western lifestyle pattern in varying intensity to the prevalence of atopic diseases in 5 small villages on Karkar Island, in northeast Papua New Guinea.
Two hundred forty-eight native people from 5 villages on tropical Karkar Island have been included in this study. The degree of Western lifestyle was assessed (questionnaire and observation) for each village. The prevalence of atopic diseases was evaluated by personal and family history, physical and dermatological examination, skin prick test (10 allergens), and measurement of total and specific immunoglobulin E levels (20 common allergens).
The more easily accessible and thus more "modern" and westernized coastal villages showed a significantly higher prevalence of habitants suffering from atopic diseases than a traditional mountain village (6.8% vs 0.0%, P = 0.034, Fisher exact test). A total of 4.4% (11/248) of the examined islanders suffered from an atopic disease. Atopic eczema seems to be absent on Karkar Island.
The results of this study suggest that so-called Western lifestyle may contribute to the development of atopic diseases.
Keywordsallergy prevalence atopic disease modern versus traditional lifestyle Westernization infections parasites public health tropics Papua New Guinea Karkar Island
What is the prevalence of atopic diseases in the absence of typical Western lifestyle?
Is there a higher prevalence of atopic diseases in traditional societies when aspects of Western lifestyle have already been introduced to a certain extent?
We included 5 villages with a total of 248 islanders in this survey: Gaubin, Kurum, and Kavailo, representing the more modern coastal villages, and Gamog, representing a traditional mountain village, a 4-hour walk from the shore. The village Did is in an intermediate position, as it is situated a little further inland, between the 3 coastal villages and Gamog (2-hour walk from the shore).
The study was conducted on Karkar Island, Papua New Guinea. The inhabitants are divided into 2 linguistic groups: The Takia in the South and the Waskia in the North of the island. Data were collected in 1996/97 and 2001 in 5 different Takia villages: Gaubin, Kurum, and Kavailo on the Coast; Did a little further inland; and Gamog on the slopes of the Mount Kunugui volcano.
Considering the total number of inhabitants in the 5 villages, a representative percentage of persons have been included in the study: 31.0% (26/84) of the population of Gaubin, 8.1% (62/765) of Kurum, 17.3% (60/347) of Kavailo, 8.0% (42/525) of Did, and 16.2% (58/358) of Gamog. Altogether 248 randomly selected volunteers took part in the study (convenient sample). They were approached directly in their home villages. Resources for the study were limited, yet in all villages most people were keen on participating--despite skin tests and blood sampling. Only the first people who appeared after being in-formed by traditional acoustical means (Garamut wood drum) could be included in the study. The average age was 25.7 (± 15.2) years; 9% (23/246) of the subjects were children under the age of 10. The percentage of women was 53% (132/248) and that of men 47% (116/248). The following data were obtained on each of the participants.
General Medical and Allergy History
A detailed medical history consisting of 29 questions and focusing on atopic diathesis, personal and family history of atopic diseases, general health, utilization of Western drugs, and general life conditions (standardized, self-developed questionnaire, validated in 30 patients with atopic disease) was obtained. The answers were translated from Neo-Melanesian Tok-Pidgin to German and English.
Skin Prick Tests
Skin prick tests (SPT) were performed at the volar side of the lower forearm of the participants and the wheal diameters were read after 20 minutes. Histamine and 0.9% sodium chloride were used as controls. Seven aeroallergens (Artemisia vulgaris, grass-pollen mixture, Dermatophagoides pteronyssinus, Dermatophagoides farinae, dog epithelium, cat epithelium, and rat epithelium) and 3 food allergens (hen's egg, codfish, and cow's milk) were tested (Allergopharma, Reinbeck, Germany). Additionally, we included SPT results against cockroach collected in 2001-2002. Wheal diameters of more than 3 mm were considered positive.
Total and Specific Immunoglobulin E
The evaluation of medical histories and the SPT were followed by blood sampling directly in the villages. Within a maximum time of 4 hours--depending on the location of the village--the samples were transported to Gaubin Hospital in a cooled container. In the laboratory of the hospital the blood was centrifuged and sera were stored frozen until total and specific immunoglobulin E (IgE) measurements were performed at the Department of Dermatology and Allergy Biederstein, Technical University München, Munich, Germany. The Pharmacia CAP System IgE fluorescent enzyme immunoassay was used. Specific IgE to 20 different allergens was evaluated quantitatively with the Pharmacia CAP System radioallergosorbent test (RAST) fluorescent enzyme immunoassay. The results are given in RAST classes from 1 to 6. The following 20 allergens were measured: D. pteronyssinus, D. farinae, dog epithelium, cat epithelium, rat epithelium, pig epithelium, egg protein, cow's milk protein, codfish (Cadus morua ), sweet potato (Ipomea batatas), bastard mackerel (Trachurus japonicus), mango (Mangifera indica), banana (Musa sapientum/paradisiaca), papaya (Carica papaya), arabic gum, timothy grass (Phleum pratense), mugwort (Artemisia vulgaris), cockroach (Blattella germanica), latex (Hevea brasiliensis), and Ascaris lumbricoides.
The medical examination focused on clinical signs of atopic airway diseases (such as rhinoconjunctivitis, rhinitis, and dyspnea) and skin manifestations of allergy or atopy. The frequency and extent of symptoms and the correlation of the medical history of clinical signs and allergen exposure were recorded and stigmata of atopy were registered. We considered that a person was suffering from an atopic disease by combining the allergy history with SPT and RAST results.
The following analytical statistical tests were applied: as a parametric test, the Student t test; as a nonparametric test, the Wilcoxon rank sum test; and for noninterval data, the χ2 test/Fisher exact test. All medical histories, translations from Neo-Melanesian Tok-Pidgin, SPT, and total and specific IgE measurements were conducted by the same examiner.
1. General Lifestyle and Health Conditions on Karkar Island
2. Traditional Lifestyle in the Mountain Village Compared with the Coastal Villages
Infections and Lifestyle Variables in Coastal and Mountain Villages: Significant Differences
P < 0.01
P < 0.01
Respiratory tract infection
P < 0.05
Chronic back pain
P < 0.005
P < 0.05
No significant differences between mountain and coastal villages were found concerning the following parts of the medical histories: prevalence of atopic diseases in family history, smoking habits, use of betel nut, tuberculosis, malaria, and ear infections. There was no significant overall difference with respect to total IgE, SPT results, and specific IgE against aeroallergens (Herbert et al, in preparation).
3. Low Prevalence of Atopic Diseases on Karkar Island
The overall prevalence of atopic diseases in the 5 investigated villages on Karkar Island was 4.4%. Thus, only 11 of the 248 examined islanders suffered from rhinoconjunctivitis and/or asthma. No atopic eczema was observed and there were no medical histories of signs of atopic eczema either. Stigmata of atopy were difficult to evaluate and showed no significant differences between areas.
4. Skin Prick Test and Specific IgE Results
The 3 most common aeroallergen sensitizations were the following: 16.4% of the villagers (40/244) showed a positive SPT against D. pteronyssinus, 15.4% (22/143) against cockroach, and 1.2% (3/243) against grass-pollen mixture. This order was reflected by the RAST results. As already mentioned, anti-Ascaris IgE was present in 82% (203/248) of the blood samples.
5. Prevalence of Atopic Diseases in the Mountain Village Compared with the Coastal Villages
Prevalence of Atopic Manifestations; Rhinitis/Rhinoconjunctivitis, Allergic Asthma, and Atopic Eczema in the Coastal, Intermediate, and Mountain Villages
Atopic Disease (Total)
6. Significant Differences between Subjects with and without Atopic Diseases
In the group of islanders suffering from an atopic disease, 25% of the people worked in typical Western occupations, whereas in the group of islanders without an atopic disease only 12.7% did. Yet this difference was not significant (Wilcoxon test). Western occupations include the following: employees of the Western health system, teachers, pastors, and shopkeepers. Traditional occupations are as follows: farmers, workers in coconut plantations, fishermen, and persons without a specific occupation.
Furthermore, people suffering from atopic disease took significantly (P < 0.05) more acetylsalicylic acid than people without atopic disease (Wilcoxon test). Villagers with atopic disease used acetylsalicylic acid 20.4 times a year, whereas people without atopic disease stated to take this drug just 12.0 times a year (arithmetic mean). Antibiotics (eg, amoxicillin and chloramphenicol) were used in a similar pattern by subjects with and without atopic disease and by subjects in coastal and mountain villages.
The results of this study suggest that a traditional lifestyle may protect against atopic diseases. Yet 1 major limitation of this investigation is the rather small sample size. Nevertheless, the selected villages were quite representative for the population on Karkar Island. A multivariate analysis was not performed.
1. The Traditional Lifestyle on Karkar Island
As 83% of the adults lived on subsistence gardening, lack of physical exercise--so typical for industrialized countries --is not a problem on Karkar Island.
Except for cooking fires, there is no other source of air pollution. It has been suggested that within large families like those on Karkar Island the probability of developing an atopic disease would be decreased . Traditionally, children are breast-fed over long periods of time and the use of milk powder just started to spread over the island slowly since approximately 2000. Breast-feeding has been shown to decrease the development of atopic diseases . Traditions generally retain an important role, including the importance of the clan structure, the celebration of traditional feasts, the chewing of betel nut, the use of traditional herbal medicine, and--despite evangelization--the broad belief in magic and sorcery (Herbert, Dietrich Reimer Verlag in print, English edition in preparation).
Among the many aspects of traditional life, which may stimulate the immune system of the islanders, infections play a predominant role. The area is highly endemic for plasmodium falciparum, vivax, and ovale. Therefore, people develop a partial immunity to these protozoa. Although malaria sometimes can be life threatening (especially for children), symptoms are mostly only moderate and may be misinterpreted as a cold. Thus, a malaria attack within the last 12 months might have affected even more than 82% of the islanders. The broad IgE sensitization against A. lumbricoides seems to widely reflect current helminth infestations. Stool samples from the Gaubin Hospital laboratory and data from an investigation carried out in Kevasob village on Karkar Island  support this suggestion. Furthermore, the prevalence of hookworm infestation (Ancylostoma duodenale/americanus) is even higher than the prevalence of infestation with A. lumbricoides. Infections with Strongyloides stercoralis are found as well. Considering these facts, most of the islanders will have suffered from 1 or even several nematode infestations within the last 12 months. Helminths are known to exert a substantial influence on the host's immune response  and results of an investigation by Hagel et al  carried out on Venezuelan children suggest that the formation of specific anti-Ascaris IgE reflects an effective immune response to these parasites.
In addition to parasitic infestations, bacteriological infections are also extremely common. Pyodermas of different kinds, and the already mentioned chronic respiratory infections, were observed in many islanders. When the percentage of islanders whose immune system was actually confronted with mycobacteria is being estimated, it has to be taken into account that the manifestation index of tuberculosis is only under 10% . Thus, more than 90% of tuberculosis infections entail a clinically unapparent immune stimulation (subclinical infection). Chronic dermatophyte and yeast (Pityriasis versicolor) infections are immunomodulatory as well .
The following numbers give the best idea of the eminent immune-stimulating role of infections on Karkar Island. Just 3% of the subjects (7/248) had none of the abovementioned 6 infections. Furthermore, we have to take into account the broad variety of other common infections like pneumonia, viral hepatitis, frambesia tropica (Yaws), pyodermas, mastitis puerperalis, scabies, urogenital tract infections, gonorrhea, pyelonephritis, tooth problems, and gastritis. Thus, we conclude there is not a single islander not suffering from 1 or more infections.
2. Low Prevalence of Atopic Diseases on Karkar Island
The low overall prevalence of atopic disease on Karkar Island (4.4%) cannot be explained by a lower allergen load. The tropical environmental conditions on the island are likely to entail a high load of various natural antigens, which are often the cause of allergic diseases in Western countries. House dust mite, cockroach, animal epithelia, and mold allergens may be prevalent. This assumption is supported by the RAST results. Most of the subjects showed specific IgE antibodies against environmental antigens. The traditional lifestyle seems to protect the Karkar Islanders from developing atopic diseases--interestingly, despite ongoing specific IgE production. One possible explanation would be that the traditional lifestyle lowers the impact of IgE on effector cells (eg, mast cells and basophils).
3. Traditional Lifestyle and Low Prevalence of Atopic Diseases in the Mountain Village Compared with the Coastal Villages
The hypothesis that a traditional lifestyle protects against atopic diseases is further supported by the coincidence of the more modern lifestyle of coastal villagers and their significantly increased risk of developing atopic diseases. Some aspects of a more traditional way of life in the remote mountain village Gamog may be repeated in short: In Gamog there are no electricity, no cars, no asphalt streets, no chemicals, almost no use of industrially produced foods, and less influence of Western medicine. The geographical and partial social isolation of the mountain village Gamog and the retention of traditional gardening practices has already been described by King et al. . The significantly increased number of mountain villagers keeping pets can also be regarded as an indicator of a traditional lifestyle. Considering all lifestyle variables, differences between villages were most striking in the field of infections: the number of dermatophyte infections, worm infestations, and severe respiratory tract infections were significantly higher in the mountain village compared to those in the coastal villages.
The more traditional lifestyle in the isolated mountain village was correlated with a significantly lower prevalence of atopic diseases: actually, no atopic disease at all was found in the mountain village where typical aspects of modern Western lifestyle were absent. Yet in the 3 easily accessible and more modern coastal villages, the prevalence of atopic diseases (rhinitis/rhinoconjunctivitis and asthma) was 6.8% (10/148). As in Western countries, the most common mani-festation of an atopic disease on Karkar Island was rhinitis/rhinoconjunctivitis.
Another finding is that in a period of 22 years there was a significant increase (P < 0.05) in the reported asthma prevalence (extrinsic and intrinsic asthma) in the coastal villages: from 1.5% in 1974  up to 4.7% in 1996. In the traditional mountain villages the prevalence of asthma seems to have remained unchanged. The higher prevalence of atopic diseases in the more accessible coastal villages could be due to the rise of Western influence in recent decades.
4. Lifestyle Differences of Karkar Islanders Suffering from an Atopic Disease
Lifestyle differences of Karkar Islanders suffering from an atopic disease compared with nonatopic subjects suggest a link between modern lifestyle and atopic diseases as well. Islanders suffering from an atopic disease tended to work more often in typical Western occupations. Furthermore, they took significantly more acetylsalicylic acid. This does not mean that the drug itself causes atopic diseases, although nonsteroidal anti-inflammatory drugs can enhance histamine release, but acetylsalicylic acid may be regarded as an indicator for a more modern lifestyle and increased Western contact. Just 1 person (excluded) indicated taking acetylsalicylic acid to relieve atopic symptoms. Therefore, the abovestated difference cannot be explained as a consequence of the treatment of atopic diseases with acetylsalicylic acid.
The idea that an increase in Western influence may also increase the prevalence of atopic diseases was already supported by Dowse, Turner, and co-workers in 1985. They showed a correlation between the increasing prevalence of asthma and the introduction of blankets in the Papua New Guinea highlands . However, Western textiles are not likely to be the only trigger for the development of allergies and they cannot explain the higher prevalence of atopic diseases in the coastal villages of Karkar Island. Meanwhile, Western textiles are widespread in all villages on Karkar Island. Nevertheless, there seems to have been a significant increase in the prevalence of atopic diseases in the coastal villages where a multitude of different aspects of Western lifestyle have been introduced. There is also evidence from Western countries suggesting that retaining a more traditional lifestyle in the farmhouse (Bavaria, Germany) or having an anthroposophic lifestyle (Steiner school children) may be accom-panied by a lower incidence of atopic diseases.
In summary, the results of our observations in the islanders of Papua New Guinea support the notion that a traditional lifestyle may protect against atopic diseases. The exact mechanisms and the most relevant single factors remain to be elucidated in future studies.
Supported by: Deutsche Gesellschaft für Allergologie und Klinische Immunologie, Germany.
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