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. 2023 Jul 20;18(7):e0283206. doi: 10.1371/journal.pone.0283206

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

Jake Hecla 1,2,*, Erik Kambarian 2, Robert Tubbs 3, Carla McKinley 1, Aaron J Berliner 1,4, Kayla Russell 5, Gabrielle Spatola 6, Jordan Chertok 7, Weston Braun 8, Natalia Hank 9, Courtney Marquette 5, Jennifer Betz 2, Terry Paik 2, Marie Chenery 2, Alex Cagan 10, Carl Willis 11, Tim Mousseau 6
Editor: Norman J Kleiman12
PMCID: PMC10358910  PMID: 37471331

Abstract

This report describes a two-year effort to survey the internal 137Cs and external β-emitter contamination present in the feral dog population near the Chernobyl nuclear power plant (ChNPP) site, and to understand the potential for human radiation exposure from this contamination. This work was performed as an integral part of the radiation safety and control procedures of an animal welfare oriented trap-neuter-release (TNR) program. The measurement program focused on external contamination surveys using handheld β-sensitive probes, and internal contamination studies using a simple whole-body counter. Internal 137Cs burden was measured non-invasively during post-surgical observation and recovery. External β contamination surveys performed during intake showed that 21/288 animals had significant, removable external contamination, though not enough to pose a large hazard for incidental contact. Measurements with the whole-body counter indicated internal 137Cs body burdens ranging from undetectable (minimum detection level ∼100 Bq/kg in 2017, ∼30 Bq/kg in 2018) to approximately 30,000 Bq/kg. A total of 33 animals had 137Cs body-burdens above 1 kBq/kg, though none posed an external exposure hazard. The large variation in the 137Cs concentration in these animals is not well-understood, could be due to prey selection, access to human food scraps, or extended residence in highly contaminated areas. The small minority of animals with external contamination may pose a contamination risk allowing exposures in excess of regulatory standards.

Introduction

On April 26th, 1986, reactor four at Chernobyl nuclear power plant suffered a catastrophic accident, breaching the reactor building and venting approximately 1.3 EBq of radioactive material into the environment over the following weeks [1]. Over thirty years later, the quantities of radioactive material present in the environment in regions of Ukraine, Belarus, and Russia pose a threat to human health [24]. Likewise, wild animal populations in these regions maintain high body-burdens of radioisotopes such as 137Cs and 90Sr[59]. During the evacuation of population centers near the power plant subsequent to the accident, a large number of domestic animals were released [10]. Despite early efforts at culling the population [11], these animals reproduced rapidly, leading to an enduring population of feral dogs and cats within the exclusion zone. Though highly accurate population estimates are not available, manual survey methods performed by Clean Futures Fund suggest approaching 1000 dogs were present in the immediate vicinity of Chernobyl Nuclear Power Plant in the spring of 2017.

Prior to the invasion by Russian forces in February 2022, the exclusion zone was an active work-site with an electrical switch-yard and extensive cleanup and stabilization activities [12, 13]. Due to the notoriety of the site, there has existed a large tourist presence in the last decade, with visitors numbering in the tens of thousands visiting Pripyat and the exclusion zone every year [14]. While the dogs in the exclusion zone are popular with invited visitors and locals, there are long-running concerns about the risks the feral dog may pose to workers and tourists [15]. Human-animal interaction in the Chernobyl exclusion zone is widespread, and the risks posed by external exposure and contamination transfer have only been studied to a limited extent. Depending on circumstances, the animals may pose a physical threat, biohazard (rabies, in particular), or radiological hazard. While often appearing friendly, the animals at the site are feral, and pose a bite risk to workers and tourists, as well as generating concern about animal welfare.

As a consequence of living in a contaminated environment, these animals may accumulate radioactive dust, move contaminated soil or objects, and transfer contamination to workers or tourists who interact with them [5, 11, 16]. Transfer of external contamination to hands or clothing may create exposure hazards that persist long after a visit to the site. This contamination may be inhaled or ingested, greatly increasing the incurred dose [17]. Site personnel have expressed concerns that highly contaminated animals may even pose a direct, external exposure hazard with prolonged interaction. However, to date no large studies of internal and external radioactive body-burden have been made, and these risks have remained largely un-quantified.

In an attempt to stabilize the population and reduce the risk of bites, Clean Futures Fund (CFF, https://www.cleanfutures.org/, along with partners such as the The Society for the Prevention of Cruelty to Animals—International (SPCAi, https://www.spcai.org/) operated a trap-neuter-release (TNR) program in the exclusion zone between 2017 and 2019. To better understand and limit the radiation dose to personnel and workers, monitoring and survey programs were developed to track volunteer dose and to understand the source term associated with the animals. These personnel safety programs had the additional benefit of producing data on animal radioactivity that may be more widely applied to radiation protection outside the clinical setting. These efforts to characterize the transfer of radioisotopes from the animals may be of growing importance as the Chernobyl Exclusion Zone seeks to increase its industrial capacity and develop a solar power station [14, 18]. These activities will dramatically increase the instances of interaction between humans and the feral dogs of Chernobyl.

Methods

This investigation focused on establishing estimates of external and internal radioactivity of dogs captured in the Chernobyl exclusion zone. This program focused first on rapidly and safely assessing external beta- and gamma-emitter contamination of animals at the entry to the clinic, and later assessing the 137Cs body burdens of the animals during the recovery phase of the neuter and vaccination process. The measurements performed on the animals were non-invasive and served the immediate purposes of assuring personnel safety and informing future radiation control procedures for similar clinics.

Ethical review and approval for the animal study was conducted with the permission of the Chernobyl Nuclear Power Plant authorities under the supervision of licensed veterinarians and veterinary technicians. A letter of support detailing the cooperation between the CFF and the Chernobyl NPP was signed by the NPP acting general director V.A. Seyda and can be found in the Github outlined below. Approval for access the exclusion zone was handled and granted by the Exclusion Zone Authority. Data collected for this paper were gathered adventitiously while animals were being treated by the medical program and as such are exempt from IACUC approval. Further, the radiation control and measurement activities described in this study were necessary measures for personnel safety during the animal-welfare project.

External contamination survey

External contamination on animals was assessed at clinic entry to prevent transfer of contamination to “clean” areas of the building. Prior to shaving and intake to surgery, the animals were “frisked” with a Ludlum model 26-2 probe held within 1cm of the fur surface to determine if any external contamination was present [19]. A threshold of 100cpm was used as the minimum count rate (with probe stationary) above which decontamination was needed before dogs could progress through the clinic. Assuming equal distribution over the area below the detector, this threshold is equivalent to a 90Sr concentration of approximately 1Bq per square centimeter.

Several animals demonstrated persistently elevated count rates on extremities that did not respond to washing or shaving. This was interpreted as internal contamination (likely in bone) due to radioisotopes like 90Sr. This finding is discussed further in results.

Whole-body contamination assessment

The whole body counter experiment was intended to quantify 137Cs body-burden in the captured animals in the post-surgical phase of the clinic. This measurement was taken during the “recovery” period following surgery in which animals must be monitored. The basic arrangement of this system consisted of a shielded, high-efficiency NaI(Tl) detector placed close to the flank of the animal being measured. Gamma-ray spectroscopy was used to identify the 137Cs photopeak and to subtract background.

The whole-body counter system described in this project used two different detector and shielding arrangements. Due to material transportation constraints, the 2017 phase of the experiment used a thick lead “apron” with rather than a full enclosure as originally intended. The shielding apron consisted of 500 lbs of lead in the form of bricks, which were arranged to create a low-background pad in a corner of the clinic. This consisted of a 2” thick lead apron with a 6” high rim around three sides placed in the lowest-background corner of the clinic, which was then designated the post-surgical recovery area. A frame made of 80-20 extrusion was used to position and hold the cylindrical NaI(Tl) detector at an adjustable height above the animal The first ten or so animals were measured with a volunteer holding the NaI(Tl) detector, rather than using the frame. Measurements were taken by positioning the probe within 2 cm of the animal’s chest with a disposable paper barrier in place to prevent contamination transfer. Gamma rays were counted using a Berkeley Nucleonics SAM940 equipped with a 3” right-cylindrical NaI(Tl) probe, which has a resolution of approximately 8% FWHM at 662keV in this application.

Due to the distribution of contamination in the clinic (mostly on the floor, below plastic sheeting), this arrangement of lead lowered the background in the 137Cs peak from approximately 50 cps to lower than 18cps with the detector elevated 15cm over the center of the lead apron. Background measurements were re-assessed frequently due to the possibility of contamination, which was mitigated using removable cardboard sheets. Simulation and measurements described in the methods section established a sensitivity threshold of approximately 100Bq/kg for this method of measurement.

In 2018, the system design was revised to improve background rejection and increase sensitivity. This system included an aluminum 80/20 structure to support 1/2in lead shielding on all sides. The enclosure measured 28”W × 28”H × 36” D. The floor of the detector assembly was lined with approximately 500 lbs of lead bricks from the prior system, and a “detector niche” was built to shield the sides and back of the NaI(Tl) cube with 3” of lead (leaving one side open to align with the dog’s center of mass). Though the lead wall thickness was limited by the quantity of lead available and the stress limits of the enclosure, the background suppression achieved was significantly improved with respect to the lead apron system. A Harshaw 4” NaI(Tl) cube scintillator read out using a URSA-II 4096-channel MCA was used for data acquisition. In this configuration, peak resolution at 662 keV was approximately 10% FWHM. The background rate measured with this system was approximately 15 cps in the Cs peak (in comparison with an unshielded background of approximately 150 cps), and boasts a factor of 3 improvement in sensitivity over the 2017 system.

The lack of graded-Z shielding in both system designs limited the ability of the system to see low-energy features such as the 59 keV emission line from 241Am and the numerous low-energy lines from 239Pu which may have been present. The high-energy 137Cs line, was easily observed due to the optical-thinness of the dogs and the high detection efficiency of NaI(Tl) at that energy. As a result, this study was limited to Cs, though future investigations using improved shielding and higher resolution detectors could expand this work to other isotopes of interest.

Monte Carlo simulations and calibration

Monte Carlo photon transport calculations were performed to determine the correlation between photopeak counts and 137[Cs] body burden for the detector and shielding designs described here. Though methods exist to use the equilibrium concentration of 40K as an in vivo calibration, the abundance of K in the surrounding concrete in the clinic made this method prone to error. To provide a consistent calibration for animals of any weight, a model was created using measurements of the torsos of four animals from the cohort. This model was then used to create input geometries representing animals weighing between 1 and 35 kg.

These torso models used International Commission on Radiation Protection (ICRP) specifications for cortical bone and skeletal muscle tissue. Though some portions of the anatomy were removed for simplicity, the mean free path of 662 keV gamma rays in tissue is significantly longer than the characteristic dimensions of any animal surveyed, rendering these changes unlikely to contribute significantly to error. Two different input templates were developed for each whole body counter version. These simulations provide a calibration allowing count-rates to be related to 137Cs body burdens without use of a phantom or the 40K ratio comparison, which is subject to extreme variation due to building materials near the detector.

Data processing

Gamma-ray spectra from each dog were recorded, along with information on animal ID number, tag number, weight and comments on decontamination status or significant medical conditions. Background measurements were performed frequently, and noted in a laboratory notebook to compensate for any contamination entering or leaving the clinic area.

A MATLAB script was used to read the spectra files, and select appropriate background files for each. For each animal, counts in the 137Cs peak were summed and subtracted from the background rate for that time interval. The animals’ weights were then used to select an interpolated counts-to-body-burden conversion factor from the simulation outputs. The excess counts in the peak region were then used to determine the body burden estimate. Counting error, as well as error from weight measurements and interpolation uncertainty were included in the calculated uncertainty in the body burden.

Results

A total cohort of 252 animals were captured and treated in the clinic in 2017, and 36 were treated in 2018 (Fig 1). We note that in order to minimize variability, only measurements taken under the supervision of the lead researcher are included in this study. Due to the limited presence of the lead researcher, the 2018 data set encompasses only the measurements taken on the first two days of the 2018 TNR campaign.

Fig 1. Methods and photos.

Fig 1

(a) Diagram of experimental approach. (b) Diagram of experimental hardware and systems. Native dogs were collected and initially triaged before being measured. Numbered, thermoluminescent dosimeter-equipped ear tags (c) were place on dogs during the TNR campaign as part of a related study.

All animals entering the clinic were surveyed using a handheld β/γ sensitive Ludlum 26-2 “pancake” probe with removable alpha shield to assess external contamination hazards before clinic entry. A total of 198 animals randomly selected from the cohort of 288 were subject to observation using the whole-body counter. Captured animals ranged in mass from 0.9 kg to 35 kg, with a sex ratio of 7:3 biased towards females. We also note that animal capture technicians in the field carried pen-type (RADEX One) active dosimeters with alarm features to provide warning should they encounter highly contaminated animals that could provide an immediate radiation threat, though this was never observed in practice.

External contamination assessed with the pancake probe above threshold (defined as 100 cpm, approximately 95 Bq per 100 cm2, assuming 22% efficiency for 90Sr) was observed on 21 of 288 animals, primarily on paws and forelegs. Assuming 90Sr as the dominant beta emitter (which is true in most areas of the zone), contamination levels ranged up to 1.9 kBq per 100 cm2. We note that averages with a areal value over 100cm2 have been made for all external contamination measurements to prevent misleadingly high estimates due to highly localized contamination.

All animals with detectable external contamination were decontaminated by washing and/or shaving until surveys showed contamination below the 100cpm threshold. No clear trends based on sex, body mass, or accompanying medical conditions were apparent in either internal or external contamination measurements performed. 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, though no further investigation was made in this study. Note that these animals were included in the whole-body counter measurements, though none of them showed 137Cs burdens above the minimum detection threshold.

The external β-emitter contamination discovered on animals was found to be highly transferable, with towels, instruments, and cleanup implements requiring frequent washing due to contamination from contact with the dogs prior to decontamination. One sling used for animal transfer was found to be contaminated to approximately 900 Bq per 100 cm2 (assuming 90Sr) over most of its surface. Volunteers involved in the intake process were frequently subjected to external contamination assessments, and were occasionally found to have contamination transfer ed from animals on clothing or gloves.

Of the 198 animals examined using the whole-body counter for internal contamination, 91 were found to have measurable 137Cs contamination ranging from 30-30,000 Bq/kg. None of the spectra gathered showed clear evidence of other radioisotopes aside from 137Cs. Most animals with measured external β contamination also had measurable internal 137Cs body-burdens. This body-burden signal is unlikely to be due to remaining external contamination, as the animals had to be fully decontaminated and surveyed before entering the operating room and recovery areas. We note that external 137Cs contamination results in β-emissions which are detected with similar efficiency to 90Sr using the Ludlum 26-2 probe.

In 2017, with a limit of sensitivity of approximately 100 Bq/kg, 62/81 animals captured within the power plant boundaries were detectably internally contaminated, versus 1/82 in the exclusion zone. In 2018, with a lower sensitivity threshold of approximately 30 Bq/kg, 20/24 animals from the power plant were detectably internally contaminated, whereas 8/11 from the exclusion zone had measurable 137Cs.

The same trend was evident in external contamination. In 2017, 15/114 animals captured within the power plant boundaries were externally contaminated, in contrast with 1/138 of those outside the boundary. In 2018, 4/24 animals captured in the power plant were externally contaminated, whereas only 1/12 from the exclusion zone tested above threshold.

The most internally contaminated animals captured in the 2017 campaign were captured near the ISF-II fuel storage facility (“ISF-II” in Fig 2b). The 2018 dataset showed that the most internally contaminated animals were captured in the reactor Local Zone and near the Novarka site, both locales extremely proximate to the reactor itself (“Reactor” and “Novarka” in Fig 2b).

Fig 2. Understanding the Chernobyl region of interest.

Fig 2

(a) Map of Chernobyl exclusion zone (2016) and 10 km radius inner circle. (b) Exploded view of points of interest (orange circles) within 10 km radius inner circle centered on the ChNPP (red diamond), colored by 137Cs contamination (2014). (Access: https://harvard-cga.maps.arcgis.com/home/index.html).

Discussion

Internal and external radioisotope contamination has been observed in animals taken from both the power plant boundary and exclusion zone, with animals in the former displaying significantly higher mean levels of internal and external radionuclide contamination. No animals were measured with levels of internal contamination that would pose an external exposure hazard in passing. Contact with the most internally contaminated animals would result in an exposure rate several times that of background in the zone (assuming travel along major tourist routes), but would not violate guidelines on maximum dose rate for members of the general public (for reference, the US public is not to be exposed to more than 20μ Sv/hr). The observed external doserates are negligible in comparison with other risks posed by working in or visiting the exclusion zone.

Dogs with removable external contamination, however, were observed and are likely to pose a small internal contamination risk to humans resulting from transfer of radioactive material to skin and clothing when interacting with the dogs. This transferred contamination could easily be inhaled or ingested if proper decontamination procedures are not followed. In several cases, significant detectable activity was transferred to clothing and equipment in the “dirty” portion of the clinic, confirming that such transfer is possible.

We conclude that internally contaminated dogs are unlikely to pose an external exposure risk to persons interacting with them based on the dose rates measured in this cohort. The highest body-burden dog in this study measured approximately 1 μSv/hr on contact (after external contamination was removed, as measured with a SAM-940 equipped with a 3” NaI(Tl)) detector. While this significantly exceeds the background dose rate in much of the zone, it is very small in absolute terms. We note that patients administered internal gamma emitters in a medical setting are not to cause exposure exceeding 20 μSv in any hour on discharge, which is some 20× higher than the most active dog in the cohort [20].

In contrast to dogs with high internal body-burdens, dogs with removable external contamination may pose a handling hazard. The dominant β-emitting radioisotope at Chernobyl is 90Sr, which is a highly bioavailable calcium analogue. External contamination levels up to 1.9 kBq per 100 cm2 were observed on a cloth sling used for animal transportation. The contamination levels observed from transfer due to contact with the dogs may result in doses significantly exceeding radiation protection standards if inhaled or ingested.

While exact contamination transfer calculations are not possible in this scenario, the example of the contamination transfer to the transport sling is instructive in calculating approximate doses. Should an individual experience the same level of contamination transfer to clothing observed in the case of the sling, and go on to ingest the amount of 90Sr present in 10 cm2 of material (perhaps by wiping the corner of their mouth on a sleeve or failing to wash their hands before eating), the dose to the bone surface would be approximately 2.5 mRem (0.22 mRem committed effective dose equivalent (CEDE)). If inhaled, this quantity would result in 17.5 mRem to the lung (2.07 mRem CEDE).

Over the course of this study, most dogs from the ChNPP site (82/105) had measurable 137Cs burdens, with four dogs exceeding 10 kBq/kg. The proportion of dogs in the exclusion zone (Fig 1) which were internally contaminated was dramatically lower (9/93), and generally had body-burdens near the lower limit of detection. Due to the varying sensitivity of the WBC systems, these ratios are best broken down by year of capture (Table 1). Extensive access to clean food provided by the CFF feeding program may have contributed to an observed decrease in internal contamination levels between 2017 and 2018, though the small sample size from the 2018 campaign limits the significance of this finding.

Table 1. Instances of internal activity detection as determined by the whole-body counting experiment.

Note that the 2017 experiment had a detection threshold of approximately 100 Bq/kg, whereas the 2018 revision was sensitive to approximately 30 Bq/kg.

Location No Detectable 137Cs Detectable 137Cs Total
ChNPP, 2017 19 62 81
Exclusion Zone, 2017 81 1 82
ChNPP, 2018 4 20 24
Exclusion Zone, 2018 3 8 11
ChNPP Total 23 82 105
Exclusion Zone Total 84 9 93
Cohort Total 107 91 198

Externally contaminated dogs were significantly more common on the ChNPP site than in the exclusion zone (19/138 vs 2/150). Rates of external contamination were not significantly different between 2017 and 2018 for either the Exclusion Zone or the ChNPP site. The sites of contamination observed were primarily on paw surfaces and between pads, though a number of dogs had extensive contamination along the entire ventral surface (Fig 3a).

Fig 3. Dosimetry and analysis of wild dogs.

Fig 3

(a) 21/288 animals surveyed as part of the 2017 and 2018 programs had external contamination above the threshold (100 cpm on Ludlum 26-2, equivalent to 95 Bq per 100 cm2 area, 90Sr). The distribution of this contamination is shown here. (b) Scatter plot of the animal body-burden as a function of body mass for the 2017 (peach) and 2018 (purple) campaign. Animals in 2017 with activity less than 100 Bq/kg are excluded. Animals in 2018 with activity less than 30 Bq/kg are excluded. External contamination is shown in this plot using squares, the size of which is correlated to the reported measurement in counts per minute using the Ludlum 26-2 probe on contact.

Conclusion

Feral dogs captured in the Chernobyl Exclusion Zone and power plant premises have detectable internal and external radioisotope body-burdens which may pose a a minor radiological hazard to those interacting with the animals. The magnitude of the internal body-burden detected in the dogs ranged from undetectable to approximately 30 kBq/kg. External contamination levels ranged from undetectable to approximately 20 Bq/cm2β. While the internal 137Cs body-burden detected in the dogs did not in any case represent an exposure hazard to those handling the animals, the external contamination detected on the dogs’ fur surveyed in this study represents a potential source term for human exposure if proper radiological hygiene practices are not followed. We assess that individuals coming into contact with the animals and practicing poor radiological hygiene could be exposed to doses in excess of limits for the general public. We further determine that the risk of exposure depends on both the extent of interaction and the location in which the animals typically reside. Animals from areas near the reactor site are more likely to be contaminated, and are more likely to carry a higher radioisotope burden, as discussed. These trends hold true for both internal and external contamination.

Going forward, those coordinating and supervising work in the Chernobyl exclusion zone and power plant area should assure that workers and tourists in the areas nearest the power plant are properly cautioned on the additional unseen risks of interacting with the feral animals [21]. Future work should focus on improving the accuracy and portability of the whole-body counter system used in this investigation, as well as selecting more sensitive β-counting instrumentation.

Acknowledgments

First and foremost, we thank the administrators and staff of Chernobyl Nuclear Powerplant (SSE-ChNPP), the Chernobyl Exclusion Zone authority, the city of Slavutych and the Novarka consortium. In particular, Stanislav Shekstelo was of great assistance in this effort. Sincerest thanks for the technical support, encouragement, general assistance, and lead shielding supplies provided by Dr. Tim Mousseau’s laboratory and collaborators in Chernobyl town during the course of this project. Finally, we thank Davian Ho for his help with the graphics.

Data Availability

All data presented here is available through github: https://github.com/aaronreichmenberliner/dogsofchernobyl.

Funding Statement

This study was funded by the Clean Futures Fund. However, the authors listed under the Clean Futures Fund did not receive any compensation for their time, and no financial transactions were made or distributed to any other co-author institutions. Tubbs Nuclear Consulting provided support in the form of salary for RT. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.

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Decision Letter 0

Norman J Kleiman

27 Sep 2022

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. The conclusions drawn may have a big impact for the radiation protection of radiation workers at the Chernobyl site as well as the public.”

Again, our apologies for the delay and the need to send the manuscript out several times for re-review due to unavailability of qualified reviewers and some initial disparities between positive and negative reviews. I am pleased that the reviews now indicate only minor revision is needed.

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Additional Editor Comments :

Dr. Berliner,

Apologies for the delay in returning your manuscript. It was difficult finding bandwidth from qualified reviewers over the summer. Initially, there was some disagreement between reviews and so we subsequently asked for additional eyes on the manuscript. I am pleased to report that the majority of reviews now ask for minor revisions. We look forward to receiving a revised manuscript.

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Reviewers' comments:

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Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Partly

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: No

Reviewer #2: N/A

Reviewer #3: N/A

********** 

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Reviewer #1: Yes

Reviewer #2: No

Reviewer #3: Yes

********** 

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********** 

5. Review Comments to the Author

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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.

********** 

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Reviewer #2: No

Reviewer #3: No

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Attachment

Submitted filename: Review of Hecla et al.docx

PLoS One. 2023 Jul 20;18(7):e0283206. doi: 10.1371/journal.pone.0283206.r002

Author response to Decision Letter 0


5 Dec 2022

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.

Attachment

Submitted filename: Response Letter.pdf

Decision Letter 1

Norman J Kleiman

6 Mar 2023

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.

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Kind regards,

Norman J Kleiman, PhD

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. 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

**********

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Reviewer #2: N/A

Reviewer #3: N/A

**********

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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!

**********

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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

**********

Acceptance letter

Norman J Kleiman

30 Mar 2023

PONE-D-22-14715R1

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

Dear Dr. Berliner:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

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    Submitted filename: Review of Hecla et al.docx

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    Submitted filename: Response Letter.pdf

    Data Availability Statement

    All data presented here is available through github: https://github.com/aaronreichmenberliner/dogsofchernobyl.


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