Potential risk factors for zoonotic disease transmission among Mongolian herder households caring for horses and camels

Surveys

Between February and March 2017, 131 Mongolian herding households were surveyed in a pilot study for zoonotic disease transmission risk factors. This pilot study was part of a larger cross-sectional study investigating the disease burden of equine influenza in Mongolia. Participating households were from Arkhangai, Uvurkhangai, and Umnugobi aimags (Figure 1). In each aimag, four smaller land units called soums (Figure 3) were chosen according to the livestock density records of the soum’s agricultural administration and the availability of local veterinarian(s) for assistance. Within each soum, a convenience sampling strategy was used to select households that owned horses or camels according to the local veterinarian.

Surveys were developed in English and translated into the Mongolian language by native Mongolian researchers (Additional file 1). For survey participation, the household had either horses or camels near the ger (portable felt home; yurt) at the time of the site visit, as required by the larger study. Surveys were administered verbally to the self-identified head of the household and recorded by a trained Mongolian field staff member. Responses were translated into English for analysis.

Statistical analysis

All data were analysed using Microsoft Excel 2016 or STATA 15.0 (StataCorp LLC, 2017). Descriptive statistics were run to characterize the ages of household heads, distance and times moved by the household each year, and median number of horses, camels, and dogs per household. Chi-square or Fisher’s exact tests were used to evaluate categorical data such as the effect of aimag location on the head of the household’s smoking habits, education level, and the household’s drinking water and heating fuel source, as well as the effect of education on smoking. A one-way ANOVA with a Bonferroni correction was used to compare continuous data such as the number of times moved and distance moved by each nomadic household throughout the year. These variables had an approximately normal distribution. The number of horses per aimag was not normally distributed so a Kruskal-Wallis H test was conducted to determine if the number of horses varied by aimag. For all tests, the null hypothesis was that there were no differences between aimags. A p value ≤ 0.05 was considered statistically significant.

Head of household demographics: Age, income, education, and tobacco use

The highest education level of the head of household was most often 8th grade (n = 81; 61.8%). Uvurkhangai had more heads of household with the > 8 years of education with 32.7% (n = 16) having at least a 10th grade education and 10.2% (n = 5) having some post-secondary education. Heads of the household in Uvurkhangai were 3.6 times more likely to have at least a 10th grade education than the other two aimags (OR = 1.6–8.1; Table 1).

Tobacco use among the heads of the household varied by aimag but overall, 42.7% (n = 56) of heads of households reported smoking (Table 2). The average age to start smoking was 22. More than half (50.9%) of the heads of households who smoked used both cigarettes and loose tobacco (n = 28). Only Umnugobi (83.3%) used cigarettes more than using both types. Heads of the household in Uvurkhangai were 2.6 times more likely to use tobacco than the other two aimags (OR = 1.2–5.3). There was no significant effect of head of household education on tobacco use (p = 0.64).

Household demographics: Livestock, movement, fuel, and water source

Of the participating households, 106 cared for horses only, 11 for camels only, and an additional 14 had both horses and camels. The median number of horses cared for by a household was 40. However, horses per household ranged between 5 and 400 and 10 and 520 for camels. Three households (2.5%) had more than 200 horses. There was a significant difference in number of horses owned by aimag (p = 0.004). Camels were only present in surveyed households of Umnugobi aimag. The median number of camels per household was 70. In Umnugobi, 44% of camel-owning households (11) had between 51 and 100 camels. Two households (8%) had more than 200 camels. Participants from all aimags reported an average of 3–4 h spent with their horses or camels each day. Most families (120; 91.6%) had at least one dog, and the median number of dogs was one (Table 2).

The herding households of this study moved frequently throughout the year for water and food for their livestock. Of the 131 households, only 11 did not move during the year (8.3%). Both Arkhangai and Uvurkhangai households moved on average four times a year, while Umnugobi households moved on average five times a year (Table 2). In Umnugobi aimag, four households (13.3%) reported that they did not move, while two households (6.7%) reported ten moves throughout the year. The mean distance moved each time by the survey households was 22 km. The farthest moved by any family was 110 km in Umnugobi. There was a statistically significant difference between distance moved by the households according to their aimag (p = 0.005). Households in Umnugobi moved significantly further than those in Arkhangai (p = 0.003).

Sources for heating fuel and household drinking water were recorded for each family (Table 2). The most common heating fuel was wood, including zag. Zag is specifically a wood from the saxaul tree (Haloxylon ammodendron) in the Gobi region and was used by three households in Umnugobi. In Arkhangai aimag, most households burned wood for heat (n = 51; 98.1%) while in Uvurkhangai, most households used dried manure (n = 33; 67.3%), followed by coal (n = 26; 53.1%). In Umnugobi, almost all surveyed households used dried manure (n = 29; 96.7%). Only two households (1.5%) used electricity to heat (Table 2). Fuel source was significantly different between aimags (p < 0.001). Households in Umnugobi were 24.3 times more likely to burn dried manure for heat than the other two aimags (OR = 3.2–185.0). All study participants reported cooking inside their home or ger.

The source for household drinking water was most commonly a river at 52.7% (69) but varied significantly by aimag (p < 0.001). River water as the primary drinking water source was reported most commonly in Arkhangai with 73.1% (n = 38) and Uvurkhangai with 61.2% (n = 30) of households. In Umnugobi, a generator-powered ground well was used as the primary drinking water source in 70.0% (n = 21) of the surveyed households (Table 2). Thirty households that reported using a river as their first drinking water source also reported using either a spring or an electric well as their second water source. Households in Arkhangai were 4.2 times more likely to use a river as their primary water sources than the other two aimags (OR = 2.0–9.0).

Zoonotic risks

Of all the household livestock, we only examined the number of horses and camels (Table 2). Not all households owned the animals for which they cared. The previously mentioned study in Tov (Zhen et al. 2010) reported fewer horses on average per household at 27 horses compared to the median of 40 in our study. The median number of camels owned per household at 70 was higher than horses. The 3–4 h that households spent with their horses or camels each day included milking and preparation for horse races. Observationally, this number was given for when they were working with the horses or camels and not assumed to be consistent year-round. While making airag (fermented mare’s milk), mares are milked five to seven times a day from late June until late summer/fall, depending on geographic region (Bat-Oyun et al. 2015). Bactrian camels were milked on average for 12 months between parturition in one study with a range between 9 and 18 months (Brezovečki et al. 2015). The Umnugobi households in this study reported milking their camels twice a day. Milking requires seasonal, daily interaction with adults and young of both species. Both species are known to be reservoirs for zoonotic diseases, so herders and especially those that milk or drink milk from these animals are at increased risk of zoonoses. In other livestock species, Brucella sp., Mycobacterium sp., Salmonella sp., Listeria monocytogenes, Campylobacter sp., Coxiella burnetii, and Escherichia coli have all been transmitted in unpasteurized milk (John 2006). Little to no research has been focused specifically up mare and camel milk handling in Mongolia, as observationally noted, milk is often drunk unpasteurized, such as with milk tea.

The presence of dogs in more than 90% of the study households carries transmission risks for zoonoses, including rabies, anthrax, and echinococcosis (Odontsetseg et al. 2009, Odontsetseg et al. 2007, Ito and Budke 2015). From 2003 to 2005, the most recent years reported by the study of rabies in Mongolia, cases in dogs surpassed cases in livestock (Odontsetseg et al. 2009). Dogs also shed hydatid Echinococcus. Sheep are the primary intermediate host for echinococcosis, but other livestock and humans can also serve as an intermediate host (Jacob and Lorber 2015). This lifecycle makes herder families at high risk for echinococcosis. A review of echinococcosis in Mongolia primarily looked at human caseloads. From 1997 to 2006, community serology studies have found between 2 and 12% of people positive for Echinococcus granulosus. Studies in domestic dogs have found Echinococcus spp.-positive dogs by both serology (25%) and necropsy (35%). Humans are primarily infected by accidental ingestion of food or water contaminated with dog feces (Ito and Budke 2015).

Zoonotic risks: Tobacco use

Tobacco use is prevalent in Mongolia. Our study found that 42.7% of heads of the household smoked, which is similar to the 48% of men nationally surveyed in 2014 (Demaio et al. 2014). In that survey, more urban men smoked, which may account for the lower level seen here. Smoking has been linked with an increase in being serologically positive for zoonotic strains of influenza, both swine and equine (Larson et al. 2015, Coman et al. 2014). This has been explained by increased likelihood of contracting the virus from touching an animal or surface and then one’s mouth as well as potentially from a lowered immune system from smoking. In our study, 69.1% of people used loose tobacco, which may increase the chance of fecal-oral contamination since the tobacco is handled by either rolling it in paper or placing it in a pipe. The 2014 national study found no effect of education on tobacco use, which was also seen in our study (Demaio et al. 2014).

Zoonotic risks: Fuel and water sources

Fuel source was most commonly wood followed by dried manure. Handling manure for burning as well as using it around cooking areas may increase the risk of enteric pathogen contamination of hands and food. A review of zoonotic pathogens associated with cattle manure found that Salmonella spp., Campylobacter spp., Listeria monocytogenes, Yersinia enterocolitica, Escherichia coli, Cryptosporidium parvum, and Giardia lamblia were all spread in manure. These are known as manure-borne pathogens (Pachepsky et al. 2006, Manyi-Loh et al. 2016). A minimum of three months is needed when the air is more than 0 °C to properly kill microbes in untreated, dry manure (Manyi-Loh et al. 2016). This is problematic in Mongolia where during much of the year the ambient temperature is below 0 °C.

Our findings in Uvurkhangai were similar to those found in Tov (Zhen et al. 2010) where ~ 40% used wood and ~ 60–70% used dried manure. Arkhangai used more wood (98.1%), and Umnugobi households reported burning dried manure for heat 24.3 times more often than the other two aimags. However, Umnugobi is hotter and drier than the other study sites, which may lower the risk of transmission of disease even when more households use dried manure for fuel.

Drinking water was most commonly from a river (60–70%) in Arkhangai and Uvurkhangai and from an electric well in Umnugobi (70%). Households in Arkhangai were 4.2 times more likely to use a river as their primary water sources than the other two aimags. Umnugobi was similar to Tov (Zhen et al. 2010) aimag, where water was most commonly from a well (72.8%) and then the river (51.5%). Livestock also used similar water sources as the people. Of the manure-borne pathogens, C. parvum is considered very infectious (Pachepsky et al. 2006) and is relevant to the Mongolian setting. A major source of C. parvum from livestock, primarily cattle, is infected drinking water (Hunter and Thompson 2005). Horses are also known to carry C. parvum (Galuppi et al. 2016), and camels have been found to carry other species of Cryptosporidium (Liu et al. 2014). Cryptosporidium sp. was found in rivers in Japan and China (Xiao et al. 2012, Ono et al. 2001), but no test results have been published for Mongolia. Because of their increased use of river water, Arkhangai may be at greater risk for waterborne pathogens than the other two aimags.

In 2015, the United Nations reported that 59.2% of Mongolian rural populations used improved drinking water sources; this included covered wells (United Nations Data 2017). This was not true in our study as more than 50% used the river as a water source. However, our study participants were not randomly chosen and were limited by type of livestock owned. In our study, 48.8% had access to wells, but it is unknown how many of these wells would be considered improved. Thus, focus should be upon lowering risks for transmission of manure-borne pathogens in all rural water sources.

Limitations

All responses were self-reported leading to possible misclassification. Specifically, some participants appeared to be hesitant or unable to give an exact number of the livestock or other domestic animals associated with the household. Some people counted those only belonging to the one household, and others claimed an amount for the extended family. This discrepancy was especially true when counting the number of dogs owned by the household compared to the number observed at the household residence. In future studies, it would be suggested to ask both numbers owned and numbers on premises. Also, as all households were not chosen randomly, external validity is a concern. Since our households were chosen by the local veterinarian, it would be expected that households that were missed were more isolated and zoonotic risks for these families could potentially be higher due to a lack of sanitation and water or more livestock diseases from reduced access to veterinary care.