Radioactive contamination in feral dogs in the Chernobyl exclusion zone: Population body-burden survey and implications for human radiation exposure

Jake Hecla; Erik Kambarian; Robert Tubbs; Carla McKinley; Aaron J. Berliner; Kayla Russell; Gabrielle Spatola; Jordan Chertok; Weston Braun; Natalia Hank; Courtney Marquette; Jennifer Betz; Terry Paik; Marie Chenery; Alex Cagan; Carl Willis; Tim Mousseau

doi:10.1371/journal.pone.0283206

Peer Review History

Original SubmissionMay 20, 2022
27 Sep 2022 Decision Letter - Norman J Kleiman, Editor PONE-D-22-14715Radioactive Contamination in Feral Dogs in the Chernobyl Exclusion Zone: Population Body-Burden Survey and Implications for Human Radiation ExposurePLOS ONE Dear Dr. Berliner, Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process. On reviewer positively noted: “Thank you for the opportunity to review this interesting manuscript for PLOS One. 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(Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #1: The paper from Hecla J. et al. aims to assess internal and external contamination of feral dogs at Chernobyl and possible contamination transfer to humans. The main conclusions are that internal contamination due to accumulation of 90Sr in bones would not result in external contamination to humans interacting with the dogs for a short period of time. In contrast, dogs with removable external contamination may pose health risks to humans interacting with them caused by contamination transfer. Here are few comments and some curiosity-driven questions: - During neutering surgery, were gross tumor-like growths observed in any part of the body? Did some of the dogs look ‘’sick’’? My question relates to possible radiation-induced soft tissues cancers and/or symptomatic manifestations of osteosarcomas due to internal contamination. - It is stated that ‘’Several animals initially believed to be externally contaminated which did not respond to decontamination efforts were hypothesized to have an internal β-emitter body-burden on bone surfaces which was externally detectable. This was likely due to 90Sr deposited on bone surfaces…’’. However, in one of the boxes of Fig 3a it is reported that 1/288 dogs had contamination that could not be washed off. What is the real number? - It is not clear the information Fig 2b conveys. Please clarify or simply remove it. - Fig 2c: Was the ear tag dosimeter worn only during the TNR procedure? If not, I wonder if the dogs wouldn’t scratch their ears, and some would do so with their contaminated paws and maybe affect the dosimeter reading. - Paraphrasing from the discussion, internal contamination would not pose a health risk to ‘’passersby’’ who would not spend hours interacting with contaminated animals (and therefore exceed the limit of 20 uSv/h). However, what about veterinarians and staff of the TNR program? How long does any procedure take and how many procedures they handle a day? -Basic statistical analysis should be provided, as for example to support the statement that internal contamination level correlated with capture location. Reviewer #2: Disaster area affected by the nuclear disaster, TNR activities are important due to the overgrowth of animal population and ethical considerations. The authors analyzed internal and surface contamination of dogs protected by TNR and evaluated exposure levels of radioactivity. There are few reports of these activities internationally, and it is useful to disseminate information analyzed by academic organizations internationally. It is worth noting that this study evaluated the risk of contamination by towels and the like contaminated during dog care and the risk to workers, tourists, and other people interacting with the dog. However, unfortunately, detailed data was not shown in the paper, and the details of the data could not be confirmed at the database address shown. In order for this study to provide scientific information to interested readers, it is recommended that the paper provide details of contamination level distribution in the dog populations. Furthermore, from the viewpoint of animal ethics, it is desirable to comprehensively provide information on the health status and infectious diseases of protected dogs. I recommend that author’s activities be shared with readers, along with detailed data, statistically analyzed results, and individual health information. Reviewer #3: Overall an interesting paper with information that has not previously been reported. However, the paper would benefit from calculations of potential dose to persons handling the dogs - as presented here, it is difficult to see that this would pose an unacceptably high risk. In addition, a photo of the dog-counting setup would be helpful. ****** 6. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. 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Attachments Attachment Submitted filename: Review of Hecla et al.docx https://doi.org/10.1371/journal.pone.0283206.r001
Revision 1
5 Dec 2022 Author Response Page line Comment Abstract Even high levels of contamination rarely pose a health risk, even to those who are contaminated. Did the authors quantify the amount of contamination present on any of the dogs, calculate the amount that could reasonably transfer to a person, and determine the potential health effects of this transfer? Barring some sort of calculation to this effect, I have to confess to being somewhat dubious about the potential for external contamination on a dog to transfer to a person in sufficient quantity to pose a health risk. - The quantification of the total surface activity is in the results section, and has been amended to reflect uncertainty in transfer coefficients . While the dose caused by ingesting or inhaling this quantity of material is not large in absolute terms, it is significant above exposure thresholds in place for members of the public. We have edited the paper to reflect this 3 30 Again, I am somewhat dubious about contamination posing a health risk, even if transferred to skin. Can the authors provide some calculations based on average and maximum removeable contamination levels they found, indicating a plausible dose to the skin from incidental contact with contaminated animals, and to the whole body in the event that some of this contamination were to transfer to food and be ingested? I understand that, according to ALARA, any exposure is to be avoided if possible – but I’m also guessing that tourists and animals are likely to be unfamiliar with the ALARA principle , so such an assessment seems reasonable. -We have added this analysis to the results section. We appreciate these edits, as they significantly improve the paper. 4 34 Similarly, can the authors calculate exposure to people at a distance of, say, 30 cm and 1 m from the contaminated animals they measured? How does the calculated dose rate compare to the actual dose rates measured? -Due to the fact the emitters (the dogs) have a spatial extent comparable to the standoff distance, simple inverse square scaling does not work. As a result, we would have to run detailed particle transport calculations to answer this question properly. As the doserates are negligible for external exposure, we have modified the language to reflect the minimal nature of the hazard. 4 75 How does the background noted here compare to unshielded background count rate outside at this location? -This has been added in. It’s about a factor of ten reduction. 5 96 Do the authors have a citation for the high counting efficiency noted here? It’s not that I doubt them – just that Knoll notes an intrinsic counting efficiency of a little less than 90% for a 4” NaI detector and, when we add to that a geometric counting efficiency of 50% or less, the absolute counting efficiency is more likely around 40-45% for Cs-137. -This was phrased poorly. We were referring to the intrinsic efficiency, not the overall counting efficiency. This has been revised to clarify. 5 100 Good call on not using K-40! The amount in concrete (and brick, for that matter) depends strongly on the clay mineralogy of these materials -Thank you. We made this call after attempting this in the lab– the corrections just didn’t work well. 6 131 Can the authors provide a reference (or calculation) for 22% counting efficiency for Sr-90? Also, is this for Sr-90 alone, or are you assuming that Y-90 is in equilibrium? If Y-90 is present, the actual counting efficiency might be much higher due to the presence of the second beta and its much higher energy. -This is from the user’s manual for the Ludlum 26-2, and assumes the Y90 is in equilibrium. You are correct to point out this, and we have corrected our values to reflect an equilibrium Sr90/Y90 concentration (https://ludlums.com/images/data_sheets/M26-2.pdf) We have also included this reference in the manuscript. 7 160 How did the authors differentiate between the beta and gamma radiation when determining the counting efficiency? Or is the gamma counting efficiency simply too low to be a factor (in which case, perhaps this can be noted)? -Gamma efficiency is extremely low (<1%) for the sensor used. Further, a crude gamma/beta discrimination test (flipping the pancake to irradiate the tube from the back, which is shielded by 5mm Fe) was used on all contaminated animals to determine if significant gamma emitter contamination was present. 7 168 Here, too, calculated exposure rates would be helpful. We have addressed this in the text. Thank you for pointing this out. 8 190 Do the authors recommend that anyone coming into physical contact with animals wear gloves, wash their hands, shower, change clothing, etc afterwards to reduce their exposure? We have added this recommendation. Can the authors suggest mechanisms by which touching a contaminated animal can result in significant internal contamination and likely exposures? I can think of a few (e.g. eating a sandwich before washing one’s hands) – but this seems unlikely to transfer sufficient contamination to produce a high internal exposure. We noted multiple incidents of transfer to the hands and clothes of workers in the clinic requiring decontamination. Notes from the 2017 campaign indicate at least a half-dozen incidents of volunteers requiring clothes be changed or otherwise decontaminated due to contact with the dogs. 8 200 The paper mentions using an “energy-compensated NaI(Tl) detector. I am familiar with using energy-compensated GM detectors and have used many of them over the years. But I have never heard the term applied to sodium iodide. Can the authors indicate which of the NaI(Tl) detectors mentioned was energy-compensated? -This was an error, thank you for pointing this out. The doserate function in the SAM940 uses the gamma ray energy to determine doserate. However, this is not true “energy compensation,” and this has been removed. 8 201 Thanks for noting that 1 µSv/hr is not a very high dose rate – this might be worth mentioning in the abstract as well, even if only qualitatively. -We have added additional language to contextualize the doserate. Thank you for pointing this out! 9 217-218 I have to admit that this level of exposure doesn’t seem as though it’s anything to be worried about. I know…ALARA…but it’s also less than I recorded during a flight from NYC to LAX or from Detroit to Amsterdam. -That is correct that it’s low, but it’s above standards for exposure to the public, hence our concern. We have modified our language a bit to provide additional context. 9 237 I’m not sure that I agree with the word “hazard” given the low doss reported in this paper. ICRP notes a dose of 2-3 mrem as being a “trivial” dose of radiation and most of the doses reported here are in that range. But even a dose of, say, 1 rem gives only 0.05% risk of developing a fatal cancer – compared to the risk from driving or the background cancer mortality rate, even 1 rem does not seem like much of a “hazard.” Is there another word that can be used to indicate that there might be a risk – but that it’s very, very low? -We have amended this to state that the risk is low, but in excess of regulatory standards. This better reflects the nature of the risk, as you are correct in that “hazard” conveys too strong of a risk. Can the authors include a photograph (or at least a detailed drawing) of their canine whole-body counter (preferably with a canine being counted)? -Due to a camera containing most photos being stolen, we have a fairly limited array of photos showing the system. We have added a figure that shows the device in action, along with a head-on photo of the device. However, the head-on photo of the system unfortunately was taken when one researcher was measuring his own Cs body burden in the system. His backside has therefore been edited out of the photo, which will be mentioned in the caption. - During neutering surgery, were gross tumor-like growths observed in any part of the body? Did some of the dogs look ‘’sick’’? My question relates to possible radiation-induced soft tissues cancers and/or symptomatic manifestations of osteosarcomas due to internal contamination. -The animals did not appear “sick” in the overwhelming majority of cases, though the average age of the animals was noted to be rather low. To quote Dr. Betz: “Nothing is noted. However, must take into consideration that it is a very small incision and we reach in with a hook and pull the uterus out so we are not physically exploring the abdomen. There is a possibility of tumors in there, however, highly unlikely at that age.” - It is stated that ‘’Several animals initially believed to be externally contaminated which did not respond to decontamination efforts were hypothesized to have an internal β-emitter body-burden on bone surfaces which was externally detectable. This was likely due to 90Sr deposited on bone surfaces…’’. However, in one of the boxes of Fig 3a it is reported that 1/288 dogs had contamination that could not be washed off. What is the real number? Thank you for pointing this out, the number has been revised. Two animals (dogs O007 and O068) were contaminated. Figure 3 has been updated in the manuscript. - It is not clear the information Fig 2b conveys. Please clarify or simply remove it. Thank you for pointing this out. We have updated Figure 2 and removed the original Figure 2b. - Fig 2c: Was the ear tag dosimeter worn only during the TNR procedure? If not, I wonder if the dogs wouldn’t scratch their ears, and some would do so with their contaminated paws and maybe affect the dosimeter reading. The details about the ear tag study have been removed from the discussion. You are correct that this is a potential confounding factor, but this study is outside the scope of this paper. - Paraphrasing from the discussion, internal contamination would not pose a health risk to ‘’passersby’’ who would not spend hours interacting with contaminated animals (and therefore exceed the limit of 20 uSv/h). However, what about veterinarians and staff of the TNR program? How long does any procedure take and how many procedures they handle a day? -Procedures took between 5 and 20min. Depending on dog capture rate and clinic operations, each vet would perform between 10 and 40 procedures per day. Personal dosimeters (RADEX One) were worn by all clinic staff, and total doses did not not exceed 10uSv for any individual for any day. The highest accumulated doses were encountered by staff working in the field, rather than those in the clinic. No animals surveyed had an external doserate on contact above 1uSv/hr. As a result, the doserates at 30cm are significantly lower than that. I cannot provide doserates at 30cm and 1m without resorting to detailed modeling, as the emitter dimension is of a similar scale to the standoff distance. -Basic statistical analysis should be provided, as for example to support the statement that internal contamination level correlated with capture location. Thank you for pointing this out. We have updated the manuscript and removed the problematic statement. Reviewer #2: Disaster area affected by the nuclear disaster, TNR activities are important due to the overgrowth of animal population and ethical considerations. The authors analyzed internal and surface contamination of dogs protected by TNR and evaluated exposure levels of radioactivity. There are few reports of these activities internationally, and it is useful to disseminate information analyzed by academic organizations internationally. It is worth noting that this study evaluated the risk of contamination by towels and the like contaminated during dog care and the risk to workers, tourists, and other people interacting with the dog. However, unfortunately, detailed data was not shown in the paper, and the details of the data could not be confirmed at the database address shown. In order for this study to provide scientific information to interested readers, it is recommended that the paper provide details of contamination level distribution in the dog populations. Furthermore, from the viewpoint of animal ethics, it is desirable to comprehensively provide information on the health status and infectious diseases of protected dogs. I recommend that author’s activities be shared with readers, along with detailed data, statistically analyzed results, and individual health information. We thank the reviewer for this comment. We apologize for not uploading our materials to the referenced github sooner. All materials have been uploaded to the github including A compiled dataset (“data1.xlsx”) Jupyter notebook for plotting Figure components and construction files Photos Reviewer #3: Overall an interesting paper with information that has not previously been reported. However, the paper would benefit from calculations of potential dose to persons handling the dogs - as presented here, it is difficult to see that this would pose an unacceptably high risk. In addition, a photo of the dog-counting setup would be helpful. We thank the reviewer for this comment. We have updated the manuscript where possible and added more photos in Figure 2 of the dog-counting setup. Attachments Attachment Submitted filename: Response Letter.pdf https://doi.org/10.1371/journal.pone.0283206.r002
6 Mar 2023 Decision Letter - Norman J Kleiman, Editor Radioactive Contamination in Feral Dogs in the Chernobyl Exclusion Zone: Population Body-Burden Survey and Implications for Human Radiation Exposure PONE-D-22-14715R1 Dear Dr. Berliner, We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements. Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication. An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. 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If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation. Reviewer #2: All comments have been addressed Reviewer #3: All comments have been addressed ******** 2. Is the manuscript technically sound, and do the data support the conclusions? The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented. Reviewer #2: Yes Reviewer #3: Yes ****** 3. Has the statistical analysis been performed appropriately and rigorously? Reviewer #2: N/A Reviewer #3: N/A ****** 4. Have the authors made all data underlying the findings in their manuscript fully available? The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified. Reviewer #2: Yes Reviewer #3: Yes ****** 5. Is the manuscript presented in an intelligible fashion and written in standard English? PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here. Reviewer #2: (No Response) Reviewer #3: Yes ****** 6. Review Comments to the Author Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters) Reviewer #2: The revised manuscript entitled “Radioactive Contamination in Feral Dogs in the Chernobyl Exclusion Zone: Population Body-Burden Survey and Implications for Human Radiation Exposure (PONE-D-22-14715_R1)”, submitted by Jake Hecla et al. reported radioactive contamination in feral dogs in the Chernobyl exclusion zone and hazard to workers, tourists, and others interacting with the dogs. The health risks from internally contaminated dogs are extremely low and do not pose a public health concern. However, scientifically clarifying the impact on support staff through the activities of the authors is an important effort to deny reputational damage and excessive anxiety. Reviewer #3: I appreciate the authors taking the time and making the effort to address my comments. Interesting paper! ****** 7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files. If you choose “no”, your identity will remain anonymous but your review may still be made public. Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy. Reviewer #2: Yes: Tomisato Miura Reviewer #3: Yes: Andrew Karam ******** https://doi.org/10.1371/journal.pone.0283206.r003
Formally Accepted
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