Epidemiology of Human Populations Exposed to Aerial Bt Sprays

Shortly after the use of Bt insecticides became common in forestry, several large-scale epidemiological studies were conducted on human populations exposed to commercial formulations of Btk. In these studies, exposure of humans to Bt formulations was confirmed by a variety of techniques, including nose swabs, but there were no adverse effects attributable to the exposure in the populations exam-ined.83 84 It was later suggested that the low number of reported cases where Bt could have been a causative agent of disease were underestimated due to several factors, including inadequate diagnostic facilities, failure to identify Bt isolates, the mixed microbiological composition of some clinical specimens, and the rejection of clinically significant isolates as contaminants.5 However, even if infections attributed to other species had been attributed to Bt, there was no correlation between levels of exposure and the number of reported incidents.

Since these earlier aerial applications of Bt insecticides over residential areas, there have been several other small- to large-scale aerial applications over residential areas in which human health effects were monitored. Recent episodes of direct spraying in residential areas occupied by many thousands of humans took place in Auckland, New Zealand and Victoria, British Columbia, Canada. In the first New Zealand episode, aerial application and ground application of a Bt formulation (Foray 48B) based on Btk was initiated in East Auckland, New Zealand in October, 1996, to eradicate the white-spotted tussock moth (Orgyia thyellina), which had invaded the area from Japan.85, 86 A total of 23 aerial applications and 21 ground applications were made in the spray area, which contained approximately 30,000 households and 80,000 people. Possible effects on health due to the Bt sprays were monitored by a combination of surveys and examination of hospital and physician records. Hospital discharge data indicated there was no association between aerial spray and miscarriage or pregnancy complications, corneal ulcers, or gastrointestinal illness. In the case of gastrointestinal illness, there was an increase in cases compared to the baseline year of 1994 (21 cases vs. 2 cases). However, this increase also occurred outside the spray zone and was likely caused by changes in diagnostic practices and/or increases in reporting illnesses in general.

As an extension of the medical record surveys, medical attendance at one health care facility was monitored during October, 1996. Complaints were categorized and their frequency and nature compared to October, 1995. When the attendance data for this facility were analyzed, there was no increase in attendance during spraying. A total of 278 people at the facility complained of 682 specific symptoms during October, 1996. Respiratory symptoms comprised 40% of the complaints, followed by eye irritation or pain (31%), skin irritation or rash (30%), nonspecific general symptoms such as malaise (28%), headache (18%), and diarrhea (2%). Diagnostic laboratory records from four area hospitals were used to determine the frequency of Bt recovery from clinical samples. The microbiologists reported that Bt was identified as a contaminant in an unspecified number of occasions since the onset of spraying. Medlab Auckland recovered Bt from one eye swab and one wound swab. The eye isolate was obtained from a child with conjunctivitis and the wound swab, which was taken from a skin tear on an 80-year-old woman, also contained Staphylococcus aureus. One blood sample from Auckland Hospital contained Bt, but it was concluded that Bt was a contaminant.

A household survey was conducted in Auckland in which a total of 721 people participated (322 of the respondents lived inside the spray zone). The participants were asked if they felt that Bt sprays negatively affected them. There was no significant difference in response between residents living inside and outside the spray zone (53 inside the zone said "Yes"; 48 outside the zone said "Yes"). The survey reported that a consistently higher proportion of target area households reported eye and throat irritation, headaches, breathing difficulties, and fatigue, but did not state whether this finding was statistically significant. This study was well designed and included information on the baseline level of symptoms before spraying began. Although there is the possibility of bias associated with any survey because respondents who feel strongly about an issue are most likely to participate, this effect was nullified by inclusion of controls from outside the spray area. In the end, there was no evidence to associate Bt sprays with any gastrointestinal illness.

In January, 2002, another Bt (Foray 48B) spray program was initiated in the Auckland area of New Zealand to control the painted apple moth (Teia anartoides), a serious invasive pest of many tree species. A group of 181 volunteers self-reported any changes in how they viewed certain aspects of their health before and after the spray program was initiated.87 Following spraying, many respondents reported increases in various health criteria, such as diarrhea, irritated throat and itchy nose, and stomach problems. However, most residents reported no health problems and, importantly, there were no relevant increases in visits to various health care providers. This study should be considered flawed because it used only a self-reporting group that lacked appropriate controls, and included many individuals with self-identified health problems such as hay fever, asthma, and other allergies. The authors of this study also made the mistake of associating the occurrence of Bt spores with infection and used inappropriate statistical analyses.

In the Canadian studies, an aerial spray campaign was conducted in Victoria, British Columbia in the spring of 1999, to control the European gypsy moth (Lyman-tria dispar) with Btk (Foray 48B).88 The residential areas of Victoria were sprayed repeatedly from May 9 through June 9. Potential health and environmental effects were monitored by taking air and water samples, and nasal swabs from humans before and after the spraying, both inside and outside the areas sprayed. Nasal swabs taken a few days after the initial applications showed significant increases of Btk in human nasal swabs within, but not outside, the spray zone. However, by the end of the spray program, recovery of Btk from nasal swabs of residents both inside and outside the spray zone significantly increased. As noted earlier, the presence of Bt spores is an indication of contamination by inhalation and is highly unlikely to be due to infection. This is worth repeating because simple recovery of spores has been incorrectly interpreted as indicating infection rather than just contamination. After the Victoria spray program, follow-up studies (including analysis of emergency room visits and monitoring the possible aggravation of asthma symptoms in children) indicated no short-term health effects in the human population associated with the aerial spraying of Bt. Moreover, although Btk spores were detected in the nasal swabs, there were no subsequent reports of nasal-pharyngeal infection, suggesting that the presence of spores was transient; this is consistent with numerous animal safety studies. The authors of this study concluded that there was no short-term change in the health status of the population that had been exposed to the aerial application of Btk. A corresponding, more detailed study in the Victoria area of children with asthma — a group considered potentially more sensitive to Bt sprays — found no harmful effects of the aerial sprays.89,90

Similar epidemiological studies of children with asthma were undertaken in New Zealand after Btk spray programs during 1999-2004.91,92 Clusters of increased asthma reports were identified in some of the areas sprayed with Btk. However, these could not be directly linked to Btk because similar increases in asthma were reported in polluted areas not sprayed with Bt. These reports concluded that if Bt sprays did cause the increases in the asthma events recorded, it was due to the partic-ulate nature of the preparations sprayed aerially, not due to the biological properties of the Bt (i.e., any active growth or infection). Nevertheless, these findings do suggest that subpopulations of humans highly sensitive to particulates in the air should be adequately warned prior to aerial spraying, even though there is no indication that periodic spraying episodes with Bt lead to any long-term health effects.

Other studies have suggested possible health effects of Bt in humans, but only in workers who were routinely exposed to Bt insecticides in the course their occupations in agriculture. In these studies, no evidence of infection by Bt was found but long-term (i.e., multiple years of) exposure of greenhouse worker to Bt insecticides did lead to increases in antibody titers of IgE. Despite the presence of elevated antibody titers, none of the workers reported any adverse effects on their health.93,94

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