Epidemiology and Economic Impact of Bovine Trypanosomosis in Jawi District, Northwest Ethiopia

doi:10.21203/rs.3.rs-4687255/v1

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Epidemiology and Economic Impact of Bovine Trypanosomosis in Jawi District, Northwest Ethiopia

https://doi.org/10.21203/rs.3.rs-4687255/v1

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Background

Bovine trypanosomosis is a debilitating cattle disease considered as a bottleneck to sufficient food production and economic growth in sub-Saharan countries including Ethiopia. A cross-sectional study was carried out from November 2021 to April 2022 in the Jawi district of Northwest Ethiopia to estimate the prevalence of bovine trypanosomosis, determine the apparent density (AP) of tsetse flies, identify potential risk factors, and assess the economic impact of the disease. For the parasitological study, blood samples were collected from 384 randomly selected zebu breed cattle and examined using the buffy coat technique and Giemsa-stained thin smears. For the entomological survey, a total of 60 monoconical traps were deployed in two randomly selected kebeles. For the economic impact assessment, economic data were collected through interviews using comprehensive and pretested structured questionnaires administered to 100 households.

Results

The overall prevalence was 9.11% (95% CI = 6.43–12.45). The trypanosome species identified were Trypanosoma congolense (57.14%, n = 20), T. vivax (37.14%, n = 13) and mixed infection with T. congolense and T. vivax (5.72%, n = 2). There was a statistically significant association (p < 0.05) between sex, body condition score (BCS) and packed cell volume (PCV) of cattle and trypanosome infection, but no statistically significant differences were observed for age, coat color, altitude or kebele (p > 0.05). The mean PCV of the infected group (22.46 ± 2.56) was significantly (P < 0.001) lower than that of the non-infected group (27.77 ± 2.22). A total of 154 flies were captured, 110 tsetse and 44 other biting flies (Stomoxys, n = 26 and Tabanus, n = 18). The species of tsetse identified was Glossina tachinoides, and the apparent density was 0.61 flies/trap/day (FTD). The overall economic losses per household and per individual cattle were US$ 1,204.34 and US$ 79.55, respectively.

Conclusion

The prevalence and estimated mean total economic losses due to bovine trypanosomosis indicated that this disease is highly economically important to farmers; therefore, sustainable and integrated control methods must be be designed and implemented in this area to minimize its impact.

Biological sciences/Ecology

Biological sciences/Zoology

Bovine

Economic impact

Epidemiology

Glossina

Trypanosomosis

Ethiopia

African animal trypanosomosis (AAT) is a parasitic disease caused by unicellular protozoan parasites that belong to the family Trypanosomatidae and the genus Trypanosoma, which includes the most important species of T. congolense, T. vivax and T. brucei [1, 2]. This disease is cyclically transmitted by flies called tsetse flies, which constitute a constant threat to humans and livestock in many sub-Saharan African countries. Tsetse flies are biological and/or mechanical vectors of trypanosomes and belong to the family Glossinidae; and the genus Glossina [3, 4]. There are approximately thirty-one species and subspecies of tsetse flies that are classified into three distinct taxonomic groups mainly based on morphological features of adult genitalia: Morsitans group (subgenus Glossina), the Palpalis group (subgenus Nemorhina), and the Fusca group (subgenus Austenina) [3, 5].

AAT is likely the only disease that has profoundly affected the settlement and economic development of a major part of the continent. It occurs in 37 sub-Saharan countries covering approximately 10 million km² [6, 7]. Its occurrence is more important in Ethiopia, where agriculture makes the backbone of the economy and crop production largely depends on animal traction power [8]. More commonly the disease is caused by T. congolense, T. vivax and T. brucei and is transmitted biologically by five species and subspecies of tsetse flies, viz. G. m. submorsitans, G. pallidipes, G. fuscipes, G. tachinoides and G. longipennis that are widely distributed across the tsetse infested belts of Ethiopia between longitudes 33° and 38°E and latitudes 5° and 12° N [9, 10].

The economic importance of African animal trypanosomosis is through either direct or indirect losses. Direct losses include losses from mortality, morbidity, impaired fertility, and the costs of control and prevention operations. Thus, its impact can be manifested in terms of a reduction in outputs and costs of control and prevention [11]. In Africa, the overall economic impact of bovine trypanosomosis on total tsetse-infested land is approximately US$ 4.5 billion every year [12]. In Ethiopia, this disease threatens agricultural and cattle production more severely than any other livestock disease [13], as the disease usually affects areas with high potential for livestock-based agriculture in the country. As a result, over the past few decades, various attempts have been made to control animal trypanosomosis in tsetse belts in Ethiopia [14]. However, despite many control efforts, this disease still remains as a major animal health problem, causing considerable threats to livestock production in the country [15].

In addition, despite the existence of several studies on bovine trypanosomosis and its vectors in the country [16–41], very few studies have attempted to quantify the economic impact of the disease [42, 43], and no study on the economic impact of the disease has been performed in the current study area. In addition, quantification of the economic impact of the disease would be of paramount importance to generate evidence needed for decision making in terms of justification and prioritization of resource allocation for disease control. Therefore, the objectives of the current study were to update the epidemiology of bovine trypanosomosis and assess its economic impact in Jawi district, northwest Ethiopia.

2.1. Description of the Study Area

The study was conducted in the Jawi district of Awi Zone in the Amhara Region, Northwest Ethiopia from November 2020 to April 2021. The Jawi district covers an area of approximately 3,422.90 km² and has 31 kebeles (a subdistrict of administrative units) (Fig. 1). The study was conducted in five randomly selected kebeles of the district.

The district is classified as a lowland (‘Kolla’), with climatic conditions mainly divided into a dry season (between late November and early May) and a rainy season (from June to October). The elevation ranges from 648–1369 m. a. s. with mean annual rainfall of 1569.4 mm and a mean temperature ranging from 16.68 to 37.6°C. The vegetation types covering the area and used as habitats for many wild lives include: savanna grass land, and riverine forest and bushes, especially along the riverbanks.

Agriculture is the main livelihood of a society with mixed crop-livestock production systems in which livestock production is highly integrated with crop production. Draft oxen are mainly used for draught power, and cows are usually used for the production of milk for household consumption and sale. The cattle are mainly local breeds (Bos indicus) maintained under traditional extensive management system. According to the information obtained from the livestock development office of the district [44], there were approximately 18,640 households; and 252,211 cattle, 27,521 sheep, 62,631 goats, 22,262 donkeys, 1,388 mules, 31 camels and 122,121 poultry.

2.2. Study Population

All cattle in the herds except the very young calves that had not been taken out for grazing by the time the study was undertaken were considered as a study population. Both sex groups of local breed cattle with different age groups, body condition scores and coat colors that are maintained under traditional extensive husbandry system with communal herding constituted the study population. The age of the selected animals was determined by the dentition method provided by Torell et al. [45], and the animals were grouped into young (1–3 years), adult (4–6 years) and old (> 6 years) groups. The body condition status of the animals was assessed and categorized as poor, medium and good based on the criteria described by Nicholson and Butterworth [46]. In addition, to ensure that the coat color of the animals was a risk factor for the disease prevalence, four usual coat colors—red, white, gray and black—were considered.

2.3. Study Design, Sampling Strategy and Sample Size

This study was a cross sectional study aimed to estimate the prevalence of bovine trypanosomosis, determine the apparent density and species of tsetse flies, and assess the risk factors associated with the disease occurrence. A simple random sampling technique was employed to select the study sites (kebeles) and study animals for the parasitological study. The questionnaire survey was used to collect economic loss data from households whose cattle were used for parasitological study.

The sample size for the parasitological study was determined based on the formula ($\:n=\frac{1\cdot\:{96}^{2}{\text{P}}_{\text{e}\text{x}\text{p}}\left(1-{\text{P}}_{\text{e}\text{x}\text{p}}\right)}{{d}^{2}}$) given by [47], who assumed a 95% confidence level and 5% absolute precision, where n = the required sample size, P_exp=expected prevalence and d² = the desired absolute precision. Accordingly, a total of 384 cattle were sampled as study animals.

2.4. Methods of Data Collection

2.4.1. Parasitological study

The parasitological study involved was used to determine the prevalence and species of trypanosome parasites by using blood samples. Before starting blood sample collection, verbal informed consents were obtained from cattle owners by explaining the purpose of a procedure the and telling them the benefits a test of that is one of the definitive diagnostic test of trypanosomosis and is undertaken by collecting blood samples from the ear veins of ill cattle and looking directly at the parasites by microscope to describe a drug of choice for the disease treatment.

Once the verbal informed consent was obtained, blood samples were collected from the superficial marginal ear vein of the study cattle by pricking it with the tip of a lancet after the animal and properly secured and the site was aseptically prepared with alcohol. The blood was collected directly into heparinized microhematocrit capillary tubes to three fourths of the height and sealed at one end with crystal sealant. The collected blood samples were examined using the buffy coat technique to determine the infection prevalence and Giemsa-stained thin blood smears were used for identification of species via standard techniques [48]. The PCV of cattle was also determined from blood samples [49]. In addition to blood samples, potential risk factors for trypanosma infection such as coat color, sex, age, origin (kebele), and BCS were collected and recorded for each sampled animal.

2.4.2. Entomological study

An entomological study was carried out to determine the apparent density and species of tsetse flies at sites that seemed suitable habitats for tsetse flies, as described by the FAO [50]. Accordingly, a total of 60 monoconical traps were deployed at watering and grazing points as well as nearby grassland areas of two main rivers (Gilgelbeles and Aima) found in different kebeles of the study district. Traps were positioned in the morning at approximate intervals of 100–200 m. The underneath of trap poles was smeared with grease to prevent ants from climbing to the pole to reach the collecting cage and damage the tsetse flies. A total of 300-mL of acetone containing glass bottles with a hole in the lid; and 2-L of cattle urine containing plastic containers with an aperture cut at the side near the top were placed below ground level at approximately 30 cm from the traps. The geographic coordinates and altitudes of each trap were recorded using a hand held global positioning system (GPS).

After 72 hours of trap deployment, both tsetse and other biting flies (Tabanus and Stomoxys) were caught and counted. Tabanus and Stomoxys were identified at the genus level. Sex, species identification and apparent fly density (F/T/D) were determined for tsetse flies. However, sex differentiation of the tsetse was performed by observing their genitalia, where the enlarged hypopygium and hectors at the posterior ventral end of the abdomen were present in males and absent in females. Species identification was based on morphological characteristics, such as coloration of the tarsal segments and marking at the back of the abdominal segments. Apparent density of the tsetse was calculated as the number of tsetse catches/trap/day [50].

2.4.3. Economic study

Economic data were collected through interviews using comprehensive and pretested structured questionnaires administered to individual heads of household. The questionnaire was specifically designed for the study to gather information on quantifiable direct economic losses. The questionnaire had four sections: (1) data on losses due to milk reduction, (2) data on losses due to draft power reduction (3) data on expenditures due to treatment and (4) data on losses due to mortality at the individual household herd level.

Prior to the commencement of the interview, verbal informed consent was obtained from the selected participants who were assured of voluntary participation by explaining the purpose of the interview, the confidentiality of the response, the risks and benefits of participation in the study and the opportunity to withdraw at any time without prejudice. Then, participants were asked to describe the main clinical features that they usually observe in their cattle suffering from trypanosomosis. If their description was approximately consistent with the key words or phrases used in the veterinary literature for describing clinical signs of trypanosomosis such as loss of condition, decrease in milk yield, lacrimation, rough hair coat, weakness, depression, anaemia, salivation, nasal discharge or any combination of two or more of these symptoms, they were considered knowledgeable about the disease and were included in the interview.

To improve the cooperation of farmers, data collection procedures, including interviews, were undertaken on days free of farm work. The interviews were conducted with household heads who were owners of animals for collecting blood samples for parasitological study.

Models for estimation of economic losses due to bovine trypanosomosis:

The economic impact of the disease was estimated as the sum of the values of production losses from milk loss by affected lactating cows, values of draught power losses by the affected oxen (but not values of affected cows as they were rarely used for this purpose in the study area), values of the cattle that died of trypanosomosis (mortally losses), and the values of treatment costs in a year. Losses associated with reduced fertility, weight loss and indirect losses were not considered as the method employed for this study made it difficult to consider such variables.

Estimation of losses from milk reduction

The annual economic losses due to milk loss per household per year were calculated by using (1).

$$\:\mathbf{E}\mathbf{L}\mathbf{M}\mathbf{R}\mathbf{i}=\mathbf{N}\mathbf{C}\mathbf{i}\mathbf{*}\:\mathbf{T}\mathbf{I}\mathbf{c}\mathbf{i}\mathbf{*}\:\mathbf{F}\mathbf{I}\mathbf{c}\mathbf{i}\mathbf{*}\:\mathbf{Q}\mathbf{M}\mathbf{i}\mathbf{*}\mathbf{P}\mathbf{M}$$

where ELMRi refers to the economic losses due to milk loss in household i per year; NCi refers to the number of affected lactating cows in household i; TIci refers to the average duration of illness in days of affected lactating cows in household i; FIci refers to the average annual frequency of illness in affected lactating cows in household i; QMi refers to the average quantity of milk lost in liter per affected lactating cow per day during illness in household i; and PM refers to the average price of milk per liter.

Estimation of economic losses from draft power loss of oxen

Draft power loss was changed into monetary terms through draft power renting of animals used as a replacement for draft power loss. An ox does not work every day of the year. The probability that a day on which an ox was ill coincided with working day was calculated as the number of working days in a year divided by the number of days in a year. This was used as an adjustment factor to change the day of illness to working days of illness. The annual economic losses due to draft power loss of oxen per household per year were calculated by using (2).

$$\:\mathbf{E}\mathbf{L}\mathbf{D}\mathbf{P}\mathbf{L}\mathbf{i}=\mathbf{N}\mathbf{O}\mathbf{i}\:\mathbf{*}\mathbf{F}\mathbf{I}\mathbf{o}\mathbf{i}\mathbf{*}\left(\mathbf{T}\mathbf{I}\mathbf{o}\mathbf{i}\:\mathbf{*}\mathbf{a}\mathbf{d}\mathbf{j}\right)\:\mathbf{*}\:\mathbf{P}\mathbf{D}\mathbf{P}\mathbf{R}\:\:$$

where ELDPLi refers to the economic loss due to draft power loss for household i per year; NOi refers to the number of affected oxen in household i; FIoi refers to the average frequency of illness of affected oxen in household i; TIoi refers to the average duration of illness in a single disease occurrence in days of affected oxen in household i; adj refers to an adjustment factor; and PDPR refers to the average price of draft power replacement rent of an animal per day.

There was no clear market value for draft power replacement rent in the district, except in one kebele, Alkurand. Farmers whose oxen were unable to work had simply waited for recovery of their ill-oxen or borrowed healthy oxen from their relatives and/ or neighbors for plow. In Alkurand kebele; however, some farmers tried to have paid replacement rent for draft power, which was used to value the opportunity work output loss related to draft power loss for all households in the area.

Estimation of economic losses from mortality: Mortality losses were estimated as a function of the value of the animal by applying the price by age/sex category to the percentage mortality in each category as per recommended by [51]. There were six different categories of cattle: (1) calves, young cattle up to one year of age; (2) bulls, male animals older than one year and not castrated; (3) heifers, female animals older than one year and not inseminated or naturally mated; (4) lactating cows, cows that were milch; (5) dry cows, female cattle other than heifers and lactating cows; and (6) oxen, male cattle that were castrated and able to plow.

The economic loss estimated from the death of calves was determined only from calf-death due to the disease, despite the principle that the economic loss from the death of a calf is based on the value of calves as well as the value of the milk lost due to the early drying of lactating cows [51]. However, the economic loss estimation in the present study did not consider the loss due to early drying of lactating cows, as calves usually are not taken out for grazing before approximately 8–11 months of age (personal communication of farmers) and trypanosomosis is mostly of the tsetse-transmitted type in the area [35]. Therefore, the death of calves due to the disease was considered to have occurred after the cessation of lactation, as the average lactation length for local zebu cows is 240 days, ranging from 210 to 270 days [52]. The annual losses due to mortality were calculated by using (3).

$$\:\mathbf{E}\mathbf{L}\mathbf{M}\mathbf{i}\:=\:\left(\mathbf{N}\mathbf{C}\mathbf{D}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{C}\mathbf{D}\mathbf{i}\right)+\:\left(\mathbf{N}\mathbf{B}\mathbf{D}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{B}\mathbf{D}\mathbf{i}\right)+\:\left(\mathbf{N}\mathbf{H}\mathbf{D}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{H}\mathbf{D}\mathbf{i}\right)+\:\left(\mathbf{N}\mathbf{D}\mathbf{D}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{D}\mathbf{D}\mathbf{i}\right)+\left(\mathbf{N}\mathbf{L}\mathbf{D}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{L}\mathbf{D}\mathbf{i}\right)\:+\:\left(\mathbf{N}\mathbf{O}\mathbf{D}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{O}\mathbf{D}\mathbf{i}\right)$$

where, ELMi refers to the economic losses due to mortality for household i per year; NCDi refers to the number of calves that died from the disease in household i; PCDi refers to the average price of a single calf that died in household i; NBDi refers to the number of bulls that died in household i; PBDi refers to the average price of a head of bull that died in household i; NHDi refers to the number of heifers that died in household i; PHDi refers to the average price of a head of heifer that died in household i; NDDi refers to the number of dry cows that died in household i; PDDi refers to the average price of a head of dry cow that died from the disease in household i; NLDi refers to the number of lactating cows that died in household i; PLDi refers to the average price of a head of lactating cow in household i; NODi refers to the number of oxen that died in household i; and PODi refers to the average price of a head of ox that died from the disease in a household i.

Estimation of economic losses from treatment costs

Treatment cost constituted expenditures for therapeutic and prophylactic treatment. The annual economic loss from treatment costs was estimated by (4).

$$\:\mathbf{E}\mathbf{L}\mathbf{T}\mathbf{C}\mathbf{i}\:=\left(\mathbf{N}\mathbf{C}\mathbf{t}\mathbf{i}\:\mathbf{*}\:\mathbf{T}\mathbf{C}\mathbf{i}\right)\:+\left(\mathbf{N}\mathbf{C}\mathbf{p}\mathbf{i}\:\mathbf{*}\:\mathbf{P}\mathbf{C}\mathbf{i}\right)$$

where, ELTCi refers to economic losses from treatment costs against the disease in household i per year; NCti refers to the number of cattle treated in household i; TCi refers to the average cost of treatment per head of cattle in household i; NCpi refers to the number of cattle prophylactically treated in household i; and PCi refers to the average cost of prophylactic treatment per head of cattle in household i.

Estimation of total economic losses

The mean total economic losses due to bovine trypanosomosis per household were calculated as the sum of losses from milk loss, draft power loss, mortality, and treatment cost. Therefore, the model used to estimate the mean total economic loss is given in (5).

$$\:\mathbf{T}\mathbf{E}\mathbf{L}\mathbf{i}\:=\:\mathbf{E}\mathbf{L}\mathbf{M}\mathbf{R}\mathbf{i}\:+\:\mathbf{E}\mathbf{L}\mathbf{D}\mathbf{P}\mathbf{L}\mathbf{i}\:+\:\mathbf{E}\mathbf{L}\mathbf{M}\mathbf{i}\:+\:\mathbf{E}\mathbf{L}\mathbf{T}\mathbf{C}\mathbf{i}\:\:$$

where TELi refers to the annual mean total economic loss for household i per year; ELMRi refers to the mean economic loss due to milk reduction of lactating cows in household i; ELDPLi refers to the mean economic loss due to draft power loss of oxen for household i; ELMi refers to the mean economic loss due to cattle mortality in household i; and ELTCi refers to the mean economic loss due to the treatment cost of cattle in household i.

The mean economic loss per household was estimated by summing up all mean total economic losses estimated for each household and dividing by the number of all households involved in the study, i.e. 100 households (6).

$$\:\mathbf{M}\mathbf{E}\mathbf{L}=\sum\:_{\mathbf{i}=1}^{100}\mathbf{T}\mathbf{E}\mathbf{L}\mathbf{i}/100$$

where MEL refers to the mean economic loss per household per year; and TELi refers to the mean total economic loss in household i.

The mean economic loss per head of cattle was determined by dividing the annual mean total economic losses in the district per year by the total number of study animals in the district as shown in (7).

$$\:\mathbf{E}\mathbf{L}\mathbf{H}=\mathbf{T}\mathbf{E}\mathbf{L}/\mathbf{T}\mathbf{N}\mathbf{C}\mathbf{i}$$

where ELH refers to the mean economic loss per head of cattle per year in the district, and TELi refers to the annual mean total economic loss for the district, and TNCi refers to the total number of study animals in the district.

2.5. Data Management and Analysis

Data obtained from laboratory and field investigations, as well as from questionnaire surveys, were coded and entered into a Microsoft Excel Spreadsheet. All the statistical analyses were performed using STATA statistical software version 14 for Windows (Stata Corp, 4905 Lakeway Drive, College Station, Texas). Descriptive statistics, such as the means, frequencies, and percentages were employed to compute the parameters of the questionnaire survey for economic loss assessment. The prevalence was estimated as the number of positive individual animals divided by the total number of individuals sampled and multiplied by 100. The associations of the dependent variable (bovine trypanosomosis) with BCS and kebele were analyzed by the Chi-squared test (χ²). The associations of disease occurrence with other independent variables such as sex, age, coat color, and altitude, were analyzed by using multivariable logistic regression analysis. Goodness of fit was checked by Hosmer and Lemeshow statistics. Independent t-test was used to compare the mean PCV values of the parasitemic and aparasitemic animals. The test result was considered significant when p < 0.05 at the 95% confidence interval.

Ethical considerations

The study protocol was reviewed and approved by the Department of Veterinary Science, Research, and Animal Ethics Committees under the 1/92/1-1-1 reference number at Bahir Dar University, Ethiopia. Before taking blood samples from the animals, a brief explanation of the study and a discussion of it were given to the owners of the animals, and each owner provided signed informed permission. Blood samples were collected in accordance with the procedures for research and testing animals. All methods were managed in compliance with ARRIVE guidelines (https://arriveguidelines.org).

3.1. Parasitological findings

3.1.1. Overall prevalence and trypanosome species identified

Among a total of 384 cattle examined for trypanosomosis by using the buffy coat technique, 35 were found to be positive for the disease, with an overall prevalence of 9.11% (95% CI = 6.43–12.45). There was variation in the prevalence of trypanosome infections among kebeles. The highest prevalence was recorded in Alkurand (12.5%), followed by Bambluk (9.72%), Cymida (6.94%), and Filfil (6.94%), and the lowest was recorded in Kaba (8.33%). The difference in prevalence among kebeles was not statistically significant (p > 0.05) (Table 1). Similarly, the prevalence of trypanosomosis related to BCS was determined, and there was a relatively greater prevalence of trypanosomosis in cattle with poor BCSs (16.67%) than in those with medium BCSs (6.7%) or good BCSs (5.68%), and the difference was statistically significant (p < 0.05) (Table 1).

Table 1

Prevalence of bovine trypanosomiasis in kebeles sampled in the Jawi district.
Factor	Number of animals examined	Prevalence (%)	χ²	P value
Study sites
Alkurand	96	12.5%,	2.2320	0.693
Bambluk	72	9.72%,
Cymida	72	6.94%,
Filfil	72	6.94%,
Kaba	72	8.33%
Overall	384	9.11%
BCS
Poor	102	16.67%	9.6387	0.008
Medium	194	6.7%
Good	88	5.68%

Among the trypanosome species identified by Giemsa-stained thin smears, T. congolense accounted for 57.14% (n = 20, 95% CI = 39.35–73.68), T. vivax accounted for 37.14% (n = 13, 95% CI = 21.47–55.08), and the remaining 5.72% (n = 2, 95% CI = 01–19.15) of the parasites were mixed infections of both T. congolense and T. Vivax. T. congolense was the most prevalent species at the all study sites, except for Alkurand, where the percentage of T. vivax was 66.67% (95% CI = 34.89–90.08) (Fig. 2).

3.1.2. Analysis of the association between bovine trypanosomiasis and potential risk factors

Potential risk factors, such as altitude and age, sex and coat color of cattle, were subjected to multivariable logistic regression analysis to identify putative predictors of the disease in the model. Accordingly, the sex of the cattle was found to be significantly (p < 0.05) associated with disease occurrence (Table 2). Among the 154 males and 230 females examined, 20 (12.99%, 95% CI = 8.12–19.34) and 15 (6.52%, 95% CI = 3.7–10.53) were found to be positive for trypanosome infection, respectively; males were 2.23 (p = 0.032) times more likely to be infected by trypanosomosis than females. However, age, coat color and altitude were not significantly (p > 0.05) associated with disease occurrence (Table 2). Following multivariable logistic regression analysis, the Hosmer–Lemeshow goodness-of-fit test was conducted and the results were not significant (X² = 9.63; p = 0.14), suggesting that the model fit the data.

Table 2

Multivariate logistic regression analysis of the associations between trypanosomosis and potential risk factors in Jawi district, northwest Ethiopia
Risk Factor	Category	OR	95% CI		Z	p
Sex	Female	–	–	–	–	–
Sex	Male	2.23	1.07	4.65	2.4	0.032
Age	Old	–	–	–	–	–
	Adult	0.60	0.28	1.33	-1.25	0.212
	Young	0.31	0.09	1.02	-1.93	0.054
Coat Color	Red	–	–	–	–	–
	White	0.24	0.031	1.86	-1.36	0.172
	Gray	2.34	0.84	6.53	1.62	0.105
	Black	2.10	0.89	4.92	1.70	0.089
Altitude	800–1000	–	–	–	–	–
Altitude	1001–1200	1.13	0.51	2.53	0.31	0.758
	1201–1400	1.06	0.37	3.06	0.10	0.917

3.2. Hematological findings

Assessment of PCV in the present study revealed that the overall mean PCV was 27.29% (± 2.72) in the study animals regardless of the infection status. Considering a PCV ≤ 24% as an anaemic [53], 10.94% of the study animals were found anaemic, in which 69% were parasitemic and 30% were aparasitemic. There was highly statistically significant difference (p < 0.001) between the mean PCV of parasitemic (22.46 ± 2.56%) and aparasitemic study animals (27.77 ± 2.22%) (Table 3).

Table 3

Comparison of the mean PCV among parasitemic and nonparasitemic animals
Group	n	Mean PCV ± SD	95% CI	t value	p–value
Infected	35	22.46 ± 2.56	21.58–23.34	13.28	< 0.001
Noninfected	349	27.77 ± 2.22	27.54–28.00	13.28	< 0.001

3.3. Entomological findings

In the entomological study, a total of 154 flies, 110 tsetse and 44 other biting flies (Stomoxys, n = 26 and Tabanus, n = 18) were trapped from two kebeles found in different altitudinal ranges (Table 4). The tsetse fly identified was G. tachinoides with mean overall apparent tsetse density of 0.61 F/T/D, in which shares of Bambluk and Cymida kebeles were 61.79% (FTD = 0.76) and 38.21% (FTD = 0.47), respectively.

Table 4. Distribution and abundance of tsetse and other biting flies in the district

Kebele	Altitude (masl)	No. of days	No. of traps deployed	Tsetse fly caught		Total	FTD	Other biting flies caught
				M	F			Other biting flies caught
				M	F			T	S
Bambluk	843.8	3	30	21	47	68	0.76	6	9
Cimyda	1203	3	30	17	25	42	0.47	12	17
Total			60	38	72	110	0.61	18	26

FTD= fly/trap/day; M = male; F = female; T = Tabanus; S = Stomoxys

3.4. Economic impact estimation

In the present study, the economic losses due to bovine trypanosomosis were estimated in terms of the effect of the disease on the final output of milk yield reduction and draft power loss as well as on mortality. Accordingly, mortality and output data were collected via a questionnaire survey based on farmers’ awareness of bovine trypanosomosis. All of the respondents were able to know the symptoms of bovine trypanosomosis and were considered knowledgeable about the disease.

Using the estimated mean frequency and duration of illness of 8.21 times and 11 days in lactating cows, respectively, the annual estimate of 166 liter of milk per affected cow and 512.94 liters per household was lost in the present study. The mean daily milk loss per milch cow per day was also estimated to be 0.58 liters, ranging from 1 to 3 liters. Given the estimated mean price of milk per unit of liter (i.e., 1 L of milk purchased at US$ 0.51) in the study area, the annual mean economic loss accrued due to a reduction in milk yield as a result of the disease was estimated to be US$ 259.67 (Std. Err. =24.19; 95% CI = $US 211.6–$US 307.67) per household on average, ranging from US$ 14.7 to 1,176 (Table 6). Therefore, the annual mean economic loss due to milk loss per affected lactating cow as result of trypanosomosis was estimated to be US$ 84.04 in the study area.

The economic loss due to draft power loss per household was estimated to be approximately US$ 279.67 (Std. Dev. = 214.00; 95% CI = $US 237.21–$US 322.13) (Table 6). The mean duration and frequency of illness in an ox per year were estimated to be 10.26 days, ranging from 4 to 20.14 days, and 8.16 times, ranging from 1 to 12 times, respectively. The mean cost of renting a replacement animal for the draft power lost per day was US$10, ranging from US$7.5 to 12.5. The annual mean effective working days for draft oxen were estimated to be 54.63 days, ranging from 36 to 72 days. The mean number of working days lost was obtained by multiplying the product of the mean duration of illness and the adjustment factor by the mean frequency of illness.

The study also indicated that the mean total economic loss due to cattle mortality per household was US$ 432.20 (Std. Dev. =702.12; 95% CI = 292.89–571.51) (Table 6), of which about 68.9% was due to the death of oxen and lactating cows only. The economic loss estimation due to mortality was performed as a function of the value of cattle to the percentage mortality, and by assuming that there was no salvage value after the death of cattle in the area (personal communication). The mortality rate of bovine trypanosomiasis was 7.7% (Table 5).

Table 5

Annual economic losses due to mortality by category of cattle in 100 households per year in the Jawi district
Age/sex category	No. of death/cattle population	Market price (US$)			Total economic losses per category (US$)
Age/sex category	No. of death/cattle population	Mean	Minimum	Maximum	Mean	Min	Max
Calf	8/102	110.9375	75	137.5	887.5	600	1100
Bull	11/227	464.3182	45	1000	5107.5	825	11000
Heifer	10/178	218.75	25	325	2187.5	250	3250
Dry cow	11/219	338.6363	250	450	3725	2750	4950
Milch cow	33/361	422.1591	300	500	13931.25	9900	16500
Ox	41/427	406.5789	350	500	16669.73	14350	20500
Total	114/1514	1961.4	1045	2913	43220	28675	57300

The economic losses due to treatment costs composed of therapeutic and prophylactic treatment costs per household were estimated to be US$ 149.44 and US$ 83.36, respectively, and the overall drug expenditure to purchase trypanocidal drugs per household was US$ 232.8 (Std. Dev. = 141.64; 95% CI = 204.7–260.9) (Table 6). The mean frequency of treatment was 8.2 times, which was estimated from the mean frequency of illness in lactating cows (8.21 times) and draft oxen (8.16 times) based on the trend that farmers gave at least a single treatment to each affected animal during each episode of illness.

Table 6

Summary of annual economic losses due to bovine trypanosomiasis per household per year in Jawi district
Economic loss variables	Economic loss per household (US$)			Share (%)
Economic loss variables	Mean (95%CI)	Minimum	Maximum	Share (%)
Milk yield reduction	259.67 (211.6–307.67)	14.7	1176	21.56
Draft power loss	279.67 (237.21–322.13)	23.12	1104.66	23.22
Mortality	432.2 (292.89- 571.51)	0	6325	35.89
Treatment cost	232.8(204.7–260.9)	32	775	19.33
Total economic loss	1204.34(1018.45-1390.24)	181.46	7825.915	1

This study revealed an overall prevalence of 9.11% bovine trypanosomosis in the study area, which was comparable with results reported in the northwestern part of the country by Kebede and Animut [39], Dagnachew et al. [35], and Bishaw et al. [32], who reported overall prevalence of 10.1%, 11.33% and 7.81%, respectively. The significant similarities among the findings may be due to the presence of almost similar agroecological conditions and husbandry systems [25]. Also, it was in agreement with reports of Kassian et al. [54] conducted by using similar diagnostic technique in the Kilwa district of southern Tanzania as 9.3%. However, despite the similar agroecological conditions and the husbandry systems, [36, 43] reported a slightly greater prevalence of disease in the area, accounting for 12.4% and 12.1%, respectively; this difference may be due to inconsistent tsetse and trypanosomosis control practices in different parts of Ethiopia [19].

However, the overall prevalence obtained in the present study was higher than that reported by Seyoum and Desta [55], who reported an overall prevalence of 5.47 in the Chilga district of northwest Ethiopia. The lower overall prevalence in the Chilga district could be attributed to better veterinary services and the absence of tsetse flies in the Chilga district since tsetse flies are the main agents of trypanosomosis. Additionally, the overall prevalence obtained in the present study was not in agreement with that in previous reports by Sheferaw et al. [19], who reported an overall prevalence of 1.93 in the Gamo Gofa zone. The relatively the higher overall prevalence of bovine trypanosomosis in the present study may be due to inconsistent and juvenile tsetse and trypanosomosis control interventions in the present study area compared with those in the Gamo Gofa zone [15, 56].

Generally, however, the results of this study would have been greater than they are because of the presence of uncontrolled use of trypanocidal drugs by farmers in the study area [15], and low the sensitivity of parasitological diagnostic methods [48]. The low sensitivity of the parasitological diagnostic methods was indicated by Shifaw et al. [29], who compared the Woo test with polymerase chain reaction (PCR), and reported that the overall prevalence of bovine trypanosomosis was 1.4% and 43.3%, respectively.

Trypanosome congolense was the dominant species of the genus Trypanosma in the study area, accounting for 57.14%. This predominance of T. congolense in terms of prevalence may be due to the exposure of cattle to major cyclical vectors of Glossina tachinoides, which are more efficient transmitters of T. congolense than T. vivax in East Africa [9]. The predominance might also arise from the thought that T. congolense, apart from the initial site of inoculation, is restricted to the bloodstream, whereas T. vivax and especially T. brucei are not restricted to the blood; rather they can also invade other tissues [4]. The results of the present study in terms of trypanosome species agreed with the proportional trends reported by Morrison et al. [4] and Dagnachew et al. [41] in northwestern parts of the country. Similar findings were also previously reported for Kenya and Tanzania by Karanja [57] and Kassian et al. [54], respectively. It is tempting to speculate that the transmission in the present study area is more mechanical since the absence of major habitats for tsetse flies as result of massive sugarcane (Saccharum officnarum) cultivation, which foists farmers to keep their cattle in limited pastures, could facilitate the mechanical transmission of T vivax by biting flies at this particular site.

In terms of the association between the prevalence of bovine trypanosomosis and body condition score, there was statistically difference across the good, medium and poor body condition score (P < 0.05). Cattle in good and medium body condition were 0.39 and 0.31 times less likely to harbor the parasites, respectively, than those in good body condition. This might be rooted from the nature of the disease, as it is a wasting disease resulting in a progressive loss of body condition [58], although the effect of other wasting factors such as parasitism and malnutrition could play a role in the development of poor body condition [59]. In cattle, the poorer body condition the animal is, the greater the probability that it will harbor the parasite trypanosome. On the other hand, poor body condition can also be a risk factor for trypanosomosis, as animals in poor condition can have concurrent disease and thus are at higher risk of infection by trypanosomes. As reviewed by Bishaw et al. [29], it is therefore difficult to conclude that either poor body condition predisposes animals to trypanosome infection or trypanosome infection causes a loss of body condition based on a cross-sectional study, so it should be verified by using a longitudinal study design. Generally, however, the findings of the present study are in agreement with the previous findings reported by Hunduma and Abebe [40], Sheferaw et al. [19] and Mekuria and Gadissa [36].

A significant difference was observed in the prevalence of trypanosomosis between the different sex groups of cattle during the study period. Similar finding were reported by Mekuria and Gadissa [36] in the northwestern part of the country. The higher prevalence of bovine trypanosomosis observed in male animals might be because of male animals were more subjected to travel long distances for draught power purpose in areas where the tsetse challenge is higher. However, there was no significant difference (P > 0.05) between cattle of different age groups, although the highest prevalence of the disease was observed in old animals while young animals were found to be least infected. The highest rate of occurrence in old cattle could be associated with chronic nature of the disease for; and the lowest prevalence of trypanosomosis in young animals might be due to the effect of maternal immunity on trypanosomosis [34, 60]. Similar findings were also reported by Dagnachew et al., [15].

The study revealed that 10.94% of the study animals were found anaemic, 69% were parasitemic and 31% were aparasitemic, and the difference was highly statistically significant at P < 0.05. This findings were in line with the general understanding of anaemia and other bovine trypanosomosis studies in different parts of the country [19, 35, and 41]. On the other hand, the detection of anemia in 3l% aparasitaemic animals might suggest that other factors like malnutrition, hemoparasites and helminthes could also cause anemia in the study area [59]. Thus, the presence of individual animals infected despite of having normal PCV measurements and vice versa may help to conclude that PCV measurement alone cannot be used as a diagnostic tool for trypanosomosis in cattle [61].

The entomological findings of the present study revealed that apparent density of tsetse flies was about 0.61 flies/ trap/day, and a total of 110 G. tachinoides were identified. There was variation in apparent tsetse density between the two study sites, 0.76 FTD in Bambluk and 0.47 FTD in Cymida kebeles, which might be due to the difference in the intensity of tsetse and trypanosomosis control interventions in the kebeles. It might also pertain to the reason that as altitude decreases, apparent density of tsetse fly increases. This finding supports earlier works by Dagnachew et al. [41] who indicated that climate, which is largely influenced by altitude has an impact on tsetse populations.

The species G. tachinoides identified in the present study corroborated the findings of Mekuria and Gadissa [36] in the district. However, the overall apparent tsetse density was not in agreement with the reports of aforementioned investigators, which might be due to tsetse and trypanosomosis control interventions actively has been actively, though inconsistently, implemented in the district for five years [62]. Additionally, the overall apparent tsetse density in the present study did not agree with previous studies in other parts of the country. For instance, Regassa and Abebe [63] reported the overall apparent tsetse density to be 10.68 F/T/D in the Limu Shay tsetse infested area of the upper Didessa valley and Meharenet et al. [64] reported it to be 3.98 F/T/D in six districts along the Didessa River Basin in the Oromia region. The variation in apparent tsetse density between these previous studies and the present study might be due to differences in agro-ecological conditions, season of study and/ or onset of tsetse and trypanosomiasis control interventions in the study districts [36].

In the present study, the economic losses due to bovine trypanosomosis were assessed in households whose cattle were included in the parasitological study. It comprises four major economic variables: losses from milk yield reduction, draft power loss, mortality, and treatment cost. And, the assessment was applied in terms of the effect of disease on the final output of milk yield reduction and draft power loss as well as on mortality. Accordingly, mortality and output data were collected via a questionnaire survey based on farmers’ awareness of bovine trypanosomosis. All of the respondents were able to know the symptoms of bovine trypanosomosis and were considered knowledgeable about trypanosome infection, which is in agreement with the findings of some other previous studies, such as those of Seyoum et al. [42], Tesfaye et al. [43] and Grace et al. [65], who reported that 95.2%, 98% and 96% of the respondents were familiar with the disease in selected districts in the Baro-Akobo and Gojeb River Basins in Southwest Ethiopia, in three villages of the Metekel Zone of Northwest Ethiopia and in the cotton zone of West Africa, respectively.

Mortality losses were estimated as a function of the value of cattle as described in [51] by applying the price by age/sex category to the percentage mortality in each category, and by assuming that there was no salvage value after the death of cattle in the area (personal communication). The results revealed that the mean total economic loss due to cattle mortality per household was estimated to be US$ 432.20 (Std. Dev. =702.12; 95% CI = 292.89–571.51) (Table 6), of which about 68.9% was due to the death of oxen and lactating cows only (Table 5), which might be attributed to stress resulting from draught in oxen and lactation in the lactating cows [66]. A previous study conducted in Ethiopia by the NTTICC [67] reported an annual death of 20,000 heads of cattle out of 14.8 million heads of cattle at risk of contracting trypanosome infection, costing US$ 236 million a year. In Africa, the FAO [68] estimated direct losses of US$ 1-1.2 billion a year, in which the share of mortality was high.

In the present study, the economic losses due to treatment costs, which include curative and prophylactic treatment costs, were also estimated. The losses due to curative and prophylactic treatment per household were US$ 149.44 and US$ 83.36, respectively. Thus, the overall drug expenditure to purchase trypanocidal drugs per household in the present study was US$ 232.8 (Std. Dev. = 141.64; 95% CI = 204.7–260.9) (Table 6). The estimated economic loss due to treatment cost in the present study was higher than reported by Seyoum et al. [42] who estimated the annual average money expenditure per household per year to purchase trypanocidal drugs to be US$13 in the Gimbo and Guraferda districts of southwestern Ethiopia. The mean frequency of treatment was 8.2 times, which was estimated from the mean frequency of illness in lactating cows (8.21 times) and draft oxen (8.16 times) based on the trend that farmers gave at least a single treatment to each affected animal during each episode of illness. This finding was also generally in agreement with that of Seyoum et al. [42], who reported the mean number of treatments per individual cattle per year to be 7.4 times in the Guraferda district of southwestern Ethiopia.

However, the findings of the present study were higher than those of Tadesse et al. [30], who reported that the mean frequency of treatment for each affected cattle was 3 times per year in the Womberma district of Northwest Ethiopia; the difference in mean frequencies of treatment might be due to the difference in the burden of bovine trypanosomiasis in the present study area and the Womberma district, where prevalence of the disease was 9.11% and 2.86%, respectively. In tsetse infected areas of Africa, about 35 million curative and prophylactic treatments are given to the livestock each year, costing about US$30 million annually, from which a large majority of those treatments are likely given to cattle [12, 69].

The present study further revealed that the mean total economic loss per household was US$ 1,204.34 (Std. Dev. = 936.85; 95% CI = 1018.45-1390.24). According to the estimated mean total economic loss, mortality loss was found to be responsible for the greatest economic loss at the household level (35.89%), followed by the draft power loss (23.22%) (Table 6). The greatest share of economic loss from mortality agrees with the disease’s complication of causing cattle death in the area, where antitrypanocidal drug misuse is prevalent [15]. The total economic loss per household was variable and positively skewed (skewness = 3.8), which might indicate that few households with the largest losses played a great role in the total economic loss estimation in the area. Therefore, taking the mean total economic loss per household and per head of cattle into account, it was estimated that each household and each cattle lost about US$ 1,204.34 and US$ 79.55 per year, respectively, due to the direct losses considered in the present study as result of trypanosomosis in cattle, respectively. On tsetse-infested lands in Africa, the annual direct and indirect economic impacts of livestock trypanosomiasis have been estimated to be US$ 4.5 billion [68].

In the present study, the mean daily milk loss per milch cow was estimated to be 0.58 liter, ranging from 1 to 3 liter. Using the estimated mean frequency and duration of illness of 8.21 times and 11.01days in lactating cows, respectively, the annual estimate of 166 liter of milk per affected cow and 512.94 liter per household was lost in the present study. Given the estimated mean price of milk per unit of liter (i.e., 1 of L milk purchased by US$ 0.51) in the present study area, the annual mean economic loss accrued due to reduction in milk yield as result of the disease was estimated to an average of US$259.67 (Std. Err.=24.19; 95% CI = $US211.6–$US 307.67) per household (Table 6), ranging from US$14.7 to 1,176; the wider range pertained to the variation in yield level of the lactating cows/number of affected cows per household, the severity of milk reduction and/ or the duration of the illness. The annual mean economic loss due to milk loss per affected lactating cow as a result of trypanosomiasis was estimated to be US$84.04, which was higher than reported by Agyemang et al. [70], who reported an estimated of annual mean financial loss of US$ 16.56 per trypanosome infected N'Dama lactating cow due to reduction in milk yield in Gambia; this difference might be attributed to resistance to trypanosome infection by N'Dama cattle, albeit this is less severe under high tsetse challenge or due to lactation [71]. In the present study, it was assumed that normal amount of milk yield was returned back to the amount trypanosomosis–noninfected status after recovery [72].

In the present study, the economic loss due to draft power loss per household was estimated to be about US$279.67 (Std. Dev. = 214.00; 95% CI = $US 237.21–$US322.13) (Table 6). The mean duration and frequency of illness in an ox per year were estimated to be 10.26 days, ranging from 4 to 20.14 days, and 8.16 times, ranging from 1 to 12 times, respectively. The mean cost of renting a replacement animal for the lost draft power per day was US$10, ranging from US$7.5 to 12.5. The annual mean number of effective working days for draft oxen in the present study was estimated to be 54.63 days, ranging from 36 to 72 days, which is comparable to that reported by Goe [73] who estimated the mean number of effective working days for draft oxen in mixed farming system in Ethiopia to be 65 days a year. The mean number of days lost for draft power was estimated to be 8.16 days, ranging from 1.16 to 27.62 days; a relatively long duration of illness and a wide range might suggest the chronic nature of the disease [58], pathogenicity variability of the parasite in different individuals of cattle [74] and the number of draft oxen in each household (i.e., if excess draft oxen were present, farmers tended to wait for full recovery of their ill oxen, extending the duration of illness [75]. Thus, the mean number of days lost was obtained by multiplying of the product of the mean duration of illness and the adjustment factor by the mean frequency of illness.

The present study on economic survey also indicated that bovine trypanosomosis could cause significant annualized cattle deaths, with the mortality rate of 7.7%, which was generally in agreement with [42], who recorded a mortality rate of 6.4% in southwestern Ethiopia. The result obtained from this study was also in line with the general report of a mortality rate of 6% in Africa, where out of the 60 million cattle population at risk, 3 million cattle died each year [6, 12]. However, a lower mortality rate in cattle was recorded in Northwest Ethiopia by Tesfaye et al. [43], who reported a 4.4% mortality rate. The higher mortality rate in the present study might be pertained to the anti trypanocidal resistance prevailed now a days in the area [15].

The observation of a 9.11% prevalence in the dry season in the present study suggested that this disease is an important problem for cattle production and agricultural activity in Jawi district. The study showed that the disease was mainly caused by T. congolense followed by T. vivax, and its occurrence in the district was mainly attributed to the existence of the cyclical vector G. tachinoides, which was the predominant tsetse species with moderate apparent density. However, the study further revealed that there is potential for mechanical transmission by other biting flies, such as Tabanids and Stomoxys. The present study also revealed that the prevalence of the disease was significantly affected by age, body condition and PCV of the animal. This study further indicated that bovine trypanosomosis is an economically important disease the causes a total economic loss of US$ 1,204.34 to farmers at the household level in the district through direct impacts in terms of milk reduction, cattle mortality, draft power loss and the costs of trypanocides. Thus, the present study provides vital information on the overall epidemiology and economy of bovine trypanosomosis. Based on this conclusion, the researchers suggested the following recommendations:

Given that the control of bovine trypanosomiasis in Jawi district is important as a way to increase the incomes of farmers, concerned bodies in the country, such as the Ministry of Agriculture, National Tsetse and Trypanosomiasis Investigation and Control Institute, local government, Research Institutes, and private sectors, should collaborate in designing and implementing sustainable and integrated control programs to minimize the economic impact of the disease in the district.
As comprehensive evaluation of all costs associated with bovine trypanosomosis aids in the prioritization of the disease and recommendation of the best control methods, further research should be undertaken in the area to study the economic losses associated with reduced fertility and weight loss, as well as indirect loss of the disease.
Furthermore, sampling in the dry season, the use of a diagnostic test that has low sensitivity, and lack of assessment of trypanocidal drug resistance were considered major limitations of the present study, and need to be addressed in future studies.

Funding

No funding was received for conducting this study.

Author Contribution

Authors’ contributions • Mamo Adane was involved in the data collection and manuscript preparation• Yechale Teshome was involved in the design and implementation of the study • Wudu Temesgen was involved in the design of the study and interpretation of data• Nigatu Kebede was involved in initiation and design of the studyAll authors read and approved the final manuscript.

Acknowledgement

The authors would like to thank the cattle owners who participated in the study and the livestock sector staff of the district for providing the information needed for the study.

Data Availability

The data sets used and/or analyzed during the current study are available at https://doi.org/10.5281/zenodo.12698785

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Epidemiology and Economic Impact of Bovine Trypanosomosis in Jawi District, Northwest Ethiopia

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Abstract

Background

Results

Conclusion

Figures

1. INTRODUCTION

2. Materials and Methods

2.1. Description of the Study Area

2.2. Study Population

2.3. Study Design, Sampling Strategy and Sample Size

2.4. Methods of Data Collection

2.4.1. Parasitological study

2.4.2. Entomological study

2.4.3. Economic study

2.5. Data Management and Analysis

3. Results

3.1. Parasitological findings

3.1.1. Overall prevalence and trypanosome species identified

3.1.2. Analysis of the association between bovine trypanosomiasis and potential risk factors

3.2. Hematological findings

3.3. Entomological findings

3.4. Economic impact estimation

4. Discussion

5. Conclusion and Recommendations

Declarations

Funding

Author Contribution

Acknowledgement

Data Availability

References

Additional Declarations

Supplementary Files

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