Anthrax in the South of Russia

Introduction

Anthrax is a particularly dangerous disease belonging to the group of diseases common to humans and animals (zoonoses) and has a global distribution. In the last 25 years, in the period from 1999 to 2023, at least 16,500 cases of human diseases caused by contact with sick and fallen agricultural animals and wild animals, raw materials of animal origin, eating meat (livery) of animals involuntarily killed/fallen from anthrax have been taken into account in the world¹ [1–3]. In Russia, the situation associated with anthrax is characterized by instability against the background of a decrease in incidence. In 1999–2023, 100 outbreaks of anthrax were registered among people with more than 280 people in six federal districts of the Russian Federation: North Caucasus (North Caucasus Federal District), South (Southern Federal District), Siberian, Volga, Central and Ural Districts [2][4–6].

The south of Russia, now the territory of the Southern Federal District and the North Caucasus Federal District, historically was characterized by a high incidence of anthrax in agricultural animals and humans. This is due to intensive animal husbandry and the presence of a combination of soil and climatic conditions favorable for the existence of the causative agent of anthrax in the region. So, from 1895 to 1914, in the territory of the modern North Caucasus Federal District, more than 53 thousand heads of livestock and more than 11 thousand people fell ill with anthrax, and mortality in some years reached 23% [7]. The introduction of annual universal vaccination of livestock and specific immunization of persons with a high occupational risk of infection, as the main preventive measures against anthrax made it possible to achieve a significant reduction in the morbidity of farm animals and people; however, sporadic outbreaks of this disease continue to be registered in the Southern Federal District and the North Caucasus Federal District at present.

The purpose of the study is to analyze the current epizootic and epidemiological situation in anthrax and characterize stationary unfavorable by anthrax points (SUPs) in the south of Russia.

Materials and methods

When performing the work, we used electronic databases of SUPs and anthrax cattle burial grounds (ACBGs), developed by us on the basis of information updated in 2023 by the Rospotrebnadzor Departments for the Southern Federal District and North Caucasus Federal District, Veterinary Departments of the Southern Federal District and North Caucasus Federal District, information from the directory “Cadastre of Stationary Anthrax-Unfavorable Points of the Russian Federation”, 2005 [8], and information about ACBGs. For each subject of the Southern Federal District and North Caucasus Federal District, such characteristics were taken into account as the total number of ACBGs, the number of years of SUP activity, the specific gravity of SUPs (the ratio of the number of known SUPs to the number of settlements of the subject), the density of SUPs (the number of SUPs per 1000 km²), the frequency of manifestation of SUP activity (the number of reported outbreaks), and the number of active SUPs over the past 25 years.

When analyzing the current situation with anthrax in the south of Russia (1999–2023), the official information of Rospotrebnadzor on human incidence² and the Rosselkhoznadzor data on farm animal incidence³ were used. Due to the lack of archival data or fragmented information on the number of sick animals and people in most subjects of the Southern Federal District and some subjects of the North Caucasus Federal District, the results of a retrospective analysis of these indicators are presented in the work only for territories with the most complete information on the incidence.

Results

General characteristics of SUPs in the subjects of the Southern Federal District and North Caucasus Federal District. According to updated data, 3845 SUPs were taken into account in the South of Russia: 2589 (67.3%) in the subjects of the Southern Federal District and 1256 (32.7%) in the North Caucasus Federal District.

The leading place in terms of the number of SUPs among the subjects of the Southern Federal District and the North Caucasus Federal District is occupied by the Rostov Region, where 797 SUPs are taken into account on the territory of all 44 municipal districts (MDs). The region is characterized by high for the Russian Federation as a whole, but average for the subjects of the Southern Federal District values of density (7.89) and specific gravity (34.71%) of SUP. The first single documented foci of anthrax were dated to the beginning of the 19th century, but since 1877, accounting has become regular. There are data on 1929 outbreaks of infection that occurred over 113 years in the period of 1803–2014, while 50.44% of SUPs showed multiple activity from 2 to 15 times. However, despite such a complete accounting of the number of outbreaks, retrospective data on the disease of animals and people in the region are not available.

The second place in the number of SUPs and the leading position in terms of their specific gravity in the South of Russia belongs to the Volgograd Region. In this region, there are 727 SUPs in 37 administrative-territorial units (ATUs) of the region: in all 33 MDs and 4 urban districts (UDs), which in total make up 48.66% of the region's settlements. The density of SUPs is 6.44. During 76 active years in the period of 1900–2016, anthrax was recorded 1,445 times. SUPs with a frequency of activity from 2 to 15 times account for about 46% of points. There are only fragmentary data on the disease of 30 people and 226 livestock, including 133 cattle, 8 small cattle, and 85 pigs.

Five hundred fifty-five points in the Krasnodar Region, located in all 44 ATUs of the subject (37 MDs and 7 UDs) are unfavorable for anthrax. The specific gravity of SUPs is 31.44%, density is 7.35. From 1923 to 2011, there were 1509 outbreaks of infection over 65 years. Activity from 2 to 20 times was shown by 54.05% of SUPs. One thousand eight hundred forty-nine livestock fell ill; cattle prevailed in the structure of the species composition of animals (61.4%), small cattle accounted for 20.3%, pigs – 15.9%, and horses – 2.4%. There is no retrospective information about the disease in humans.

On the territory of the Republic of Crimea, 211 SUPs were taken into account in 13 ATUs (in 10 of 14 MDs and 3 UDs) with a specific gravity of 18.81% and a density of 7.82. During 53 years (1922–1995), the SUPs were active a total of 347 times, 51.66% of SUPs were active from 2 to 8 times. There are data on the disease of 48 people and 457 animals: 198 cattle, 103 small cattle, 5 pigs, 2 horses, and 149 other animal species (no information). The city of federal significance Sevastopol is not an unfavorable point for anthrax.

In the period from 1934 to 2008, anthrax was recorded for 43 years in 125 SUPs of the Astrakhan Region in 10 out of 11 MDs; in 27.2% of SUPs, outbreaks were reported from 2 to 14 times. The region is characterized by a low density of SUPs (2.55) and a value of their specific gravity below the average for the Southern Federal District (28.8%). In the region, 236 foci of infection were recorded, in which 906 animals died with a significant predominance of small cattle (73%), approximately equal to the proportion of cattle and pigs (11.15% and 10.82%, respectively), 4.4% of horses, and 0.66% of animals of other species. There is no archival information on the number of human anthrax cases.

In the Republic of Kalmykia, 99 SUPs were recorded in 14 ATUs (all 13 MDs and 1 UD) with a high specific gravity (37.22%) and low density (1.32). From 1956 to 2011, 266 outbreaks were reported with a disease of 126 people and 643 livestock heads (216 cattle, 396 small cattle, 23 pigs, 8 horses). The number of years of SUP activity was 46 years. Multiple activities (from 2 to 8) were observed in 60.6% of SUPs.

In the Republic of Adygea, the minimum number of points unfavorable for anthrax (75 SUPs) among the subjects of the Southern Federal District was registered on the territory of 8 ATUs: all 7 MDs and 1 UD. The specific gravity of SUPs is 32.19%, density is 9.63, being the highest value of this indicator in the Southern Federal District. In the period of 1947–1998, over 37 separate years, SUPs showed activity 167 times, 46.7% of SUPs – from 2 to 14 times. The incidence in the republic is low compared to other southern subjects, there are data on the disease of 9 people and 144 farm animals: 119 cattle, 16 small cattle, and 9 pigs.

The Republic of Dagestan is characterized by the largest number of SUPs in the North Caucasus Federal District: 516 in 41 out of 42 MDs and 7 UDs (a total of 48 ATUs), a high density (10.26) and a specific gravity (31.64%) of unfavorable points. In the 1882–2022, outbreaks of anthrax were recorded 1180 times. For 81 years of manifestations of infection, almost half of the SUPs (49.6%) were active 2–17 times. There are data on the disease of 526 people and 3601 animals dominated by small cattle (58.4%), 31% by cattle, 0.9% by horses, 0.3% by pigs, and 9.4% by other animal species (337 minks in the 1994 outbreak; 1 donkey).

The most complete information is presented in archival materials about anthrax in the Stavropol Region. This region is in second place in terms of the number of unfavorable points in the North Caucasus Federal District and has a significant specific gravity (47.56%) against the background of a relatively low density (5.46) of SUPs. In 32 ATUs (in all 26 MDs and 6 UDs), 361 SUPs were taken into account. The predominant part of SUPs (72%) showed multiple activity (from 2 to 15 times). In the region, 1227 outbreaks were recorded that took place over 89 years of the period of 1879–2022, during which 1022 people and 9829 animals fell ill. The predominance in the species structure of small cattle (60%) is due to large epizootics that occurred mainly in the late 19th – early 20th centuries; the proportion of cattle is 27.8%; 6.3% are minks (619 individuals fell ill during outbreaks in 1973 and 1977), 5% are horses, and 0.9% are pigs.

In the Chechen Republic, there are 142 SUPs located in 16 ATUs (14 out of 15 MDs and 2 UDs), with high density (8.78) and specific gravity (39.01%). The proportion of SUPs that showed multiple activity (from 2 to 20 times) was 70%. In the period of 1939–2010 for 62 years, 570 foci of infection were detected, in which 529 people were diagnosed with anthrax, 759 farm animals (small cattle – 64%, cattle – 33.2%, pigs – 2.1%, horses – 0.8%, donkey – 0.1%).

The territory of the Republic of North Ossetia-Alania is characterized by the presence of 89 SUPs with the highest density in the South of Russia (11.14); 40.45% of settlements in all 9 ATU subjects (8 MDs and 1 UD) are unfavorable for anthrax. Activity from 2 to 34 times was shown by 63% of SUPs. From 1878 to 2009, there were at least 438 outbreaks over at least 74 individual years with disease of 146 people and 1033 farm cattle with a significant predominance of cattle (97%); small cattle and pigs accounted for 2% and 1%, respectively.

In the Kabardino-Balkarian Republic, 45% of points on the territory of all 13 ATUs (10 MDs and 3 UDs) are unfavorable for anthrax, a total of 81 SUPs with a density of 6.5. From 1946 to 1999 over 47 years, SUPs showed activity 281 times, 65% of SUP – repeatedly (from 2 to 17 times). Anthrax was diagnosed in 157 people. There is information on the involvement of 136 animals in the epizootological process with an overwhelming proportion of cattle (95%); in 3.3%, the disease was reported in small cattle, and in 1.6% in other species (mink, ground squirrel).

The Karachayevo-Circassian Republic has 46 SUPs on its territory with a relatively low density for southern subjects (3.22). SUPs are 31.08% of settlements located in 11 ATUs of the subject (9 out of 10 MDs and 2 UDs). Activity from 2 to 18 times was recorded in 54.35% of SUPs. In 1923–1999 over the 45 years, 124 outbreaks were recorded: 55 cases of human anthrax and 2077 cases of animal anthrax (56 cattle, 16 small cattle, 16 pigs, 1 horse, as well as 2000 minks that fell during the epizootic in 1980).

The Republic of Ingushetia differs from other southern regions in the smallest number (21) and specific gravity (17.21) of SUPs with a density of 6.72, taken into account in 2 of 4 MDs and 4 UDs of the republic (6 ATUs). In 1956–2005 over the 33 years, the SUPs were active 96 times, 76.2% of the SUPs were active from 2 to18 times. Seventy-three people fell ill with anthrax, 136 farm cattle with a predominance of cattle fell (73.5%), small cattle and pigs accounted for 22.1% and 4.4%, respectively.

Data on the SUPs of the southern region are presented in Table 1.

On the territory of the SUPs of the southern Russia, 350 anthrax burials (ACBGs) are registered, of which 238 are in the North Caucasus Federal District, and 112 are in the Southern Federal District. Of them, 32% of ACBGs have economic affiliation, and 44% comply/partially comply with the veterinary and sanitary rules for maintenance.

Current anthrax situation in southern Russia. According to updated data, in 1999–2023, for 22 years in the South of Russia, 104 outbreaks of anthrax were registered in 92 SUPs; in 2015, 2017, and 2023 the disease was not noted. Anthrax was recorded in 12 subjects: in 7 subjects of the North Caucasus Federal District, 62 foci were detected in 55 SUPs (Republic of Dagestan – 29 foci in 26 SUPs, Stavropol Region – 10/7, Republic of North Ossetia-Alania – 9/8, Chechen Republic – 6/6, Republic of Ingushetia – 4/4, Kabardino-Balkarian Republic – 2/2, Karachayevo-Circassian Republic – 2/2); in 5 regions of the Southern Federal District – 42 outbreaks in 37 SUPs (Republic of Kalmykia – 14 outbreaks in 10 SUPs, Rostov Region – 13/12, Volgograd Region – 8/8, Krasnodar Region – 5/5, Astrakhan Region – 2/2) (Table 2).

There is evidence that during 90 outbreaks in 79 SUPs, at least 269 farm cattle fell ill; information on the number of cases of both animals and people is not available for 13 foci. In the species structure of the incidence of farm animals, cattle prevailed (224 heads, 83.3%). Small cattle accounted for 13.4% (36 heads), pigs – 2.6% (7 heads), and horses – 0.7% (2 heads). A significant complication of the epizootic situation was noted in 2010, due to a large outbreak on the farm of OOO “APC Uspensky” in the Uspenskaya village, Beloglinsky District, Krasnodar Region, with a disease of 152 cattle and 2 horses; in total, 162 farm animals fell ill with anthrax this year in 7 southern regions.

During this period, epidemic complications were recorded in 64 outbreaks in 55 SUPs with a disease of 134 people and 4 deaths. Cattle had the main epidemiological significance as a source of infection for humans, much less often infection occurred through contact with small cattle and pigs. The leading conditions of infection were contact with sick cattle not vaccinated against anthrax, in the process of care, forced slaughter, which was often carried out without notifying veterinary services, cutting and transporting carcasses, during cutting and culinary processing of meat and meat products. In all patients, the contact route of infection was realized by the development of the cutaneous form of anthrax. The secondary septic form of the disease, which complicated the course of infection in four patients, caused the development of anthrax meningitis with fatal outcomes in all cases (Republic of North Ossetia-Alania – 2 in 2006, 1 in 2007; Republic of Kalmykia – 1 in 2004). The general structure of anthrax cases was dominated by rural male residents of working age. Human diseases were recorded from March to December, the largest number of cases occurred in June-September, corresponding to the activity of the epizootic process. In 54% of outbreaks, group diseases were noted (from 2 to 6 people).

In the North Caucasus Federal District, anthrax was diagnosed in 96 people in 5 subjects. The most unfavorable epidemic situation both in the South of Russia in particular and in the Russian Federation as a whole was noted in the Republic of Dagestan, where 20 outbreaks with 66 cases of human disease were registered for 13 years (1999–2002, 2004–2005, 2010, 2012, 2018–2022). Group morbidity prevailed (2–6 people, 80%), one person fell ill only during four outbreaks. So, in 1999, 3 outbreaks with a disease of 9 people were recorded, and in 2000, 19 cases of infection were detected in 4 epidemic foci.

The second place in the number of human cases belongs to the Stavropol Region, where 8 outbreaks with a disease of 12 people were noted. In the Republic of North Ossetia-Alania, 11 people fell ill in 8 epidemic foci. During the epidemiological investigation of the outbreaks of 2006–2007, it was found that three cases of the disease with fatal outcomes in the republic were associated with contacts with patients with cattle and contaminated meat from epizootic foci in the Kursk District of the Stavropol Region. On the territory of the Chechen Republic, five patients were identified in two epidemic foci; in the Republic of Ingushetia, one outbreak was recorded with two cases of human illness.

In 5 subjects of the Southern Federal District, 25 epidemic foci with a disease of 37 people were detected during the analyzed period. In Rostov, 11 people fell ill (10 outbreaks, in 9 of which 1 person fell ill), in the Volgograd Region – 10 people during 5 outbreaks (4 – group). In the Republic of Kalmykia, 6 outbreaks were recorded (1 group – 3 people) with a disease of 8 people and 1 death, in the Astrakhan Region, 5 people fell ill in 2 foci (in one of them 4 people), in the Krasnodar Region –2 people in 2 foci (Fig. 1).

Discussion

The regions of the South of Russia have always been distinguished by a high incidence of anthrax, which continues to be a relevant infection in the modern period. Outbreaks of anthrax among animals and people have been reported in all southern regions, with the exception of Sevastopol. In the small areas of the Southern Federal District and the North Caucasus Federal District, which together make up 3.61% of the area of the Russian Federation, according to updated data, 3845 permanently unfavorable points for anthrax are concentrated, which is 11.8% of the total number of SUPs in Russia, in which 9815 outbreaks of infection were recorded. Undoubtedly, the available documentary evidence is not complete, and the official data as a whole only partially reflect the situation of the spread of anthrax among people and animals in the historical aspect.

A distinctive feature of most SUPs of the Southern Federal District and the North Caucasus Federal District is their high specific gravity and density. The average density of SUPs for these territories is 6.79, the average value of this factor is higher in the North Caucasus Federal District (7.44) than in the Southern Federal District (6.14). In accordance with the classification of SUP characteristics⁴, this indicator is low only in the Republic of Kalmykia and the Astrakhan Region (less than 3), in the Karachayevo-Circassian Republic – average (in the range from 3 to 5), and in other regions – high (more than 5), of which in some regions the density values exceed 8 (Republic of North Ossetia – Alania, Republic of Dagestan, Republic of Adygea, Chechen Republic). A high proportion (more than 20%, according to the classification) is characteristic of the SUPs of most subjects of the Southern Federal District and North Caucasus Federal District, averaging 34.63%. Moreover, in accordance with the values of this indicator in four territories (the Republic of North Ossetia – Alania, the Kabardino-Balkar Republic, the Stavropol Region, the Volgograd Region), more than 40% of the settlements of these subjects are unfavorable for anthrax. The average values of the specific gravity (up to 20%) are shown by SUPs only in the Republics of Ingushetia and Crimea.

The analysis shows that as of 2023, in accordance with the classification of SUP types [9], the vast majority of disadvantaged points (99.4%) are classified as old, 46.4% of them are nonmanifest, which have been active in the past once. Of the 92 SUPs in which outbreaks have been recorded over the past 25 years, 69 (75%) are old with a significant predominance of manifest recurrent items, in which the infection was noted twice or more (55%), over items with single manifestations (20%), and 23 SUPs (25%) – new, in which cases of anthrax disease have not been detected before. New SUPs were recorded in eight regions (Republic of Kalmykia, Astrakhan Region, Volgograd Region, Rostov Region, Republic of Dagestan, Republic of North Ossetia-Alania, Chechen Republic, Stavropol Region), while three new SUPs in the Stavropol Region, Republics of Kalmykia, and North Ossetia-Alania showed double activity.

SUPs serve as an indicator of the presence of soil foci on their territories. However, in the southern region, there is a pronounced discrepancy between the number of SUPs (3845) and registered burials of fallen animals (350), which are foci of anthrax, which indicates a significant number of unknown and, as a result, neglected ACBGs. At the same time, most of the ACBGs on veterinary records do not have balance holders (68%) and do not meet veterinary and sanitary content standards (56%), and sanitary protection zones are established only for 4.5% of ACBGs. In addition, there is a tendency to exclude ACBGs from regional registers of supervised objects. The combination of these circumstances determines the potential risk of complication of the anthrax situation in the region.

Over the past 25 years (1999–2023), anthrax epizootics have been noted in all southern regions, with the exception of the Republic of Adygea, the Republic of Crimea, and the city of Sevastopol; outbreaks among animals in the Kabardino-Balkarian and Karachayevo-Circassian Republics did not entail epidemic complications. In the Southern Federal District and the North Caucasus Federal District in 1999–2023, 64% of outbreaks of anthrax among people were registered, 46% of cases of the disease, and 50% of deaths from the total number in this period in the Russian Federation with a significant predominance of the number of epidemic foci and sick people in the Republic of Dagestan. Mortality associated with the development of secondary sepsis is due to the late availability of patients for medical care, insufficient alertness of medical personnel of medical and preventive organizations in relation to anthrax, especially its generalized forms, which led to untimely diagnosis and late initiation of adequate treatment.

Conclusion

Anthrax belongs to the significant zoonoses of the South of Russia and is almost ubiquitous in the subjects of the Southern Federal District and the North Caucasus Federal District. The epizootic and epidemiological situation for anthrax in the region continues to be unstable with periodic manifestations from sporadic cases to large epizootics and group outbreaks among people. The disadvantage of this infection is due to the presence of a significant number of soil foci, primarily old unaccounted anthrax burials, against the background of incomplete implementation of preventive measures and violation of veterinary and sanitary standards. Stabilization of the anthrax situation in the region can be achieved only with the constant implementation of a full-fledged set of preventive measures and the implementation of anti-epidemic measures in the format of interdepartmental interaction.