Determining Factors and Zootechnical Output of Biosecurity Practices in Fish Farms in the Wouri Division, Cameroon

Biosecurity practice limits the occurrence of diseases and economic losses in fish farms. The objective of this study was to characterize fish farming in the Administrative Division of Wouri, Cameroon (3°97′04″–3°58′13″N; 9°76′78″–9°46′4.3″E) and assess the biosecurity practices. A cross-sectional biosecurity audit was then conducted in 33 fish farms from March to May 2022. The “snow ball” technique, on-farm observations, and face-to-face interviews of farm managers using a semistructured questionnaire were used for data collection. The results showed that most of the fish farmers were between 18 and 40 years of age (63.64%) and not trained in fish farming (60.61%). The lack of finance (57.57%) was the main constraint to the biosecurity practice. The high fish mortality rate (>15%) was recorded in 66% of the farms. Overall, the compliance rate (CR = 40.52 ± 14.70%) and adoption rate (AR = 40.40 ± 30.10%) of biosecurity measures were intermediate. No type C farm or at the minor risk level of contamination was recorded. Farmers of 18 to 40 years of age (45.24 ± 14.75%) who attended higher school (43.83 ± 14.44%) and received training in fish farming (47.44 ± 14.39%) recorded a significant higher CR. The CR and AR were significantly higher for the isolation component (CR = 60.17 ± 19.81%; AR = 60.17 ± 25.68%) followed by traffic control (CR = 53.53 ± 25.87%; AR = 53.53% ± 34.86) and sanitation (CR = 27.70 ± 19.70%; AR = 29.84 ± 26.00%). A strong (R2 = 0.725), positive, and significant (p=0.019) linear relationship was found between the level of education of fish farmers and the biosecurity compliance rate while the health status of fish was weakly (R2 = 0.207), positively, and significantly (p=0.017) influenced by the compliance rate. Fish farming is an income-generating activity that still requires socioeconomic, technical, and institutional efforts for optimal productivity. The Cameroonian government should emphasize on the education, training, and capacity building of farmers on biosecurity practices to minimise the introduction, establishment, and spread of diseases.


Introduction
Fish farming is the main solution to meet world fsh demand. It secures food supply and poverty alleviation and as an income-generating activity, the sector employed 304,000 Africans in 2016 [1]. In Cameroon, the annual fsh mortalities and the decrease of farms productivity. Tough the evaluation of the economic impact of diseases in fsh farming has not yet been the primary concern of researchers in the developing countries [3], the economic loss caused by fsh diseases have been reported. Hence, from 2010 to 2017, reduction in salmon production and export due to necrotizing hepatopancreatitis amounted to USD 12 billion in Tailand and over USD 26 million in Viet Nam in 2015 [4].
Te failure of compliance with biosecurity measures or hygiene has been declared to be at the origin of the transmission and spread of diseases in fsh farms [5]. Biosecurity as a strategic and integrated approach that encompasses policy and regulatory frameworks aimed at analyzing and managing risks relevant to human, animal, and plant life and health, including associated environmental risks. Aquaculture biosecurity includes control of the spread of aquatic plant and animal diseases and invasive pests and the production of products that are safe to eat [6]. Tus, a sustainable management of the risks related to diseases in fsh farms requires a thorough knowledge of all the factors likely to infuence the implementation of biosecurity standards. Biosecurity is an essential tool to reduce the risk of diseases entering in a farm and suitable biosecurity practices can prevent emerging health issues, reduce impacts of disease, and improve proftability. Once the disease occurs, the treatment becomes technically and fnancially more demanding, hence the need of preventing diseases instead of a curative response [7,8]. Apart from the report of Ngueguim et al. [9] on the biosecurity practices on fsh farms in the West Region of Cameroon, no information relevant to the level of biosecurity implementation to assist policymakers in fsh industry is available although farms in Wouri Division are regularly subjected to diseases and massive mortality of fsh, namely, Nile tilapia (Oreochromis niloticus), common carp (Cyprinus carpio), and catfsh (Clarias gariepinus). Tis study was therefore designed to characterize the fsh farming and biosecurity practices, to assess the efects of the socioeconomic characteristics of fsh farmers on the implementation level of biosecurity measures, and their zootechnical consequences in the Wouri Division.

Study Area.
Te cross-sectional study was carried out from March to May 2022 on fsh farms located in the administrative subdivisions (Douala I, Douala II, Douala III, Douala IV, and Douala V) of the Wouri Division (3°97′04″-3°58′13″N; 9°76′78″-9°46′4.3″E), the Littoral Region of Cameroon ( Figure 1). Te subdivisions were selected based on the importance of fsh farming in these locations as advised by the Wouri Delegation of Livestock, Fishery and Animal Industries. Te climate is of the equatorial type with a rainy season (March-November) and a dry season (December-February). Te annual average temperature is 27.4°C and the rainfall of about 3619 mm [10].

Selection of Fish Farms.
Since the ofcial registry of fsh farms was lacking, they were frst located with the help of a local inhabitant. Te next farm was identifed using the "snow ball" technique [11] during which the manager of the previously audited farm was asked to indicate the neighboring farm and so on until the entire area was completely covered [12]. Eligibility criteria to participate in the study for fsh farms taken into consideration were road accessibility, functional status, and availability of the farm manager [5]. A total of thirty-three (33) farms were audited and codifed.

Questionnaire Design and the Biosecurity Scoring System.
Te data were collected by on-farm observations and faceto-face interviews of farm managers using a semistructured questionnaire divided into three parts. Te frst part was composed of the socio-economic characteristics of fsh farmers (age, sex, marital status, number of years of exploitation, educational level, training in fsh farming, place of training, main occupation, purpose of fsh farming, mode of land acquisition, constraints, and cost related to the biosecurity practice). Te second part entailed the zootechnical characteristics of the farm (the sanitary status of the fsh, mortality rate, and productivity) while the third section was made up of the twenty-four (24) biosecurity measures grouped into components, namely, isolation, trafc control, and sanitation [13] modifed from Arthur et al. [14] and adapted to the present study. Te questionnaire was previously tested in a subsample of seven (7) farms in the study area to verify the relevance, clarity, redundancy, and consistency of the questions. Subsequent adjustments were made accordingly. Te geographical coordinates of the farms were recorded using a GPS (the Global Positioning System).
Te linear scoring or weighting (0-1) of the biosecurity measures was used. Tus, the values 1 and 0 were assigned, respectively, to the biosecurity measure implemented or not. Te fnal score of a biosecurity measure was the sum of all the values recorded in the farms (0 or 1 per farm). Since a biosecurity component (isolation, trafc control, and sanitation) included several measures, the average score of a component was the ratio between the sum of the score of its measures and the number of biosecurity measures of the component. Te maximum score of a given measure and farm was 33 and 24 points, respectively. Te linear scoring system was empirically calculated as previously described [15][16][17][18][19]. In fact, the measures were weighted equally and any biosecurity measure estimated to be less efcient in the transmission and occurrence of a disease since fsh may sufer from poor health due to lack of implementing biosecurity measures. Te focus was on the importance of implementing biosecurity measures on the health of farmed fsh and not the level of risk generated by each biosecurity measure as it is the case in disease transmission pathways. Te weighed scoring systems in the disease transmission pathways should not have the same efciency given that direct contact is likely more risky than indirect contact with less efciency for transmitting pathogens. (1) Te ranking of the compliance rate (low, intermediate, and high) recommended by Racicot and Vaillancourt [5] was equally applied to the adoption rate and adapted to the present study to classify fsh farms (Table 1).

Statistical
Analysis. Data were stored in the Excel spreadsheet (Microsoft Ofce 2010, USA) and exported to R software for analysis. Te socioeconomic and zootechnical characteristics and the compliance and adoption rates were subjected to descriptive statistics. Te mean values of compliance and adoption rates were compared using the Kruskal-Wallis K test, the Mann-Whitney U test , and the analysis of variance (F). Te multivariate linear regression model was used to assess the relationship between biosecurity scores and socioeconomic and zootechnical characteristics of fsh farmers and farms, respectively. Biosecurity afnities (similarities) and interactions between fsh farms were determined using the principal component analysis (PCA). Te signifcance level (p) was set at 0.05.

Socioeconomic and Demographic Characteristics of Fish
Farmers in the Wouri Division. Te distribution of farms frequencies according to the socioeconomic and demographic characteristics of fsh farmers in the Wouri division ( Table 2) shows that more than half of fsh farmers (63.64%) were between 18 and 40 years of age. In addition, men (93.94%) were more involved in fsh farming. Farmers were mostly married (54.54%) and nearly 75% of them completed higher education. Out of 39.39% of farmers who received training in fsh farming, 53.85% came from the Institute of Fisheries and Aquatic Sciences (ISH), University of Douala, Cameroon. Te main constraint related to the biosecurity practice was the high cost (57.57% of

Zootechnical Characteristics of Fish Farms in the Wouri
Division. Te zootechnical characteristics of fsh farms in the Wouri division as summarized in Table 3 outline that signs of fsh diseases were observed in 42.42% of farms. Nearly, 66% of the audited farms showed a high fsh mortality rate (>15%) while few (12.12%) recorded productivity higher than 300 kg/year/m 3 .

Distribution of the Compliance Rate per Subdivisions of the Wouri Division.
Te distribution of the compliance rate per subdivisions of the Wouri division is summarized in Table 4. Te overall compliance rate (40.52 ± 14.70%) was intermediate indicating that farms were of type B or at the moderate risk level of contamination by pathogens. Te

Distribution of Farm Frequencies Relevant to the Compliance Rate of Biosecurity Components.
Te distribution of farm frequencies relevant to the compliance rate of biosecurity components as illustrated in Figure 3 indicates that globally, 18.18% and 81.81% of audited fsh farms recorded a low and intermediate compliance rate, respectively. No farm (0%) was of type C or at a minor risk level of contamination. Whatever the biosecurity component, the intermediate biosecurity practice was the most observed (75% of farms), while the poor biosecurity practice was the less implemented. Te good biosecurity practice was only observed for the isolation and trafc control implemented by 15.15% and 12.12% of farms, respectively.

Distribution of the Adoption Rate in Relation to the Biosecurity Components and Administrative Location of Fish
Farms. Te distribution of the adoption rate in relation to the biosecurity components and administrative location of fsh farms is presented in  Table 6 shows that the less adopted (0%) measures were veterinary intervention, incineration of dead fsh, and captured fsh put back into water while breeding infrastructures are layout in derivation was the most adopted (96.7%).

Distribution of the Compliance Rate in Relation to the Socioeconomic and Demographic Characteristics of Fish
Farmers. Te distribution of the compliance rate in relation to the socioeconomic and demographic characteristics of fsh farmers is summarized in Table 7. Of the characteristics studied, only age of fsh farmers, level of education, and training received in fsh farming signifcantly afected the compliance rate. Indeed, more biosecurity measures were observed by fsh farmers whose age ranged from 18 to 40 years (45.24 ± 14.75%), who attended higher school (43.83 ± 14.44%), and who received training in fsh farming (47.44 ± 14.39%).

Efects of the Compliance Rate on the Zootechnical
Characteristics of the Farms. Te efect of the compliance rate on the zootechnical characteristics of the farms is summarized in Table 8. An insignifcant (p > 0.05) increase of the mortality rate and the productivity of farms with the compliance rate of biosecurity measures were noticed. In addition, the increase of the compliance rate negatively afected (p > 0.05) the health status of fsh, while the low compliance rate rather positively infuenced (p � 0.01) the fsh health. No signifcant correlation (r � −0.00; p � 0.984) was found between the productivity of fsh farms and the cost of the biosecurity practice.

Relationship between Fish Farm Characteristics and
Implementation of Biosecurity Measures. Multivariate linear regression analysis of factors afecting the implementation of biosecurity measures in the fsh farms of the Wouri division (Table 9) shows a strong (R 2 � 0.725), positive, and signifcant (p � 0.019) relationship between the level of education and the compliance rate. Te health status of fsh was weakly (R 2 � 0.207), positively, and signifcantly (p � 0.017) infuenced by the compliance rate of biosecurity measures. A positive and nonsignifcant (p > 0.05) relationship was observed with the sex of fsh farmers, their religion, main occupation, cost of the biosecurity practice, training place, and the mortality rate. Te marital status, farm age, purpose of fsh farming, constraints related to the biosecurity practice, land acquisition method, training in fsh farming, and the farm productivity were strongly, negatively, and nonsignifcantly associated with the compliance rate of the biosecurity practice.

Biosecurity Afnities and Interactions between Fish
Farms of the Subdivisions of the Wouri Division. Te biosecurity afnities and interactions between farms of the subdivisions of the Wouri division (Figures 4(a) and 4(b)) show 95.79% of the variance in the data that was explained by the two principal component analysis (PCA) axes. Te factorial axis PCA 1 expressing 68.7% of the total variance revealed three groups of relationships between the subdivisions and the biosecurity components after projection. Te frst group including farms of Douala I and II subdivisions showed an afnity for the biosecurity components related to isolation and trafc control. Te second group of similarity included farms of Douala III and IV having an afnity for the sanitation component while fsh farms of Douala V belonging to the third group did not provide any relevant information on the biosecurity practice.

Discussion
Te results of the socioeconomic and zootechnical characteristics of fsh farming and biosecurity practices in the administrative division of Wouri, Cameroon showed that more than half of the farmers (63.64%) were between 18 and 40 years old, suggesting that this age group is young and therefore more active and productive. People over 40 years of age were less involved in fsh farming probably because either that activity was secondary or these people were less dynamic. Tis result is comparable to 28.8% of fsh farmers over the age of 40 observed by Olasunkanmi [20] in Osun State in Nigeria. Te high involvement of the youth in fsh farming is contradictory to the reports of Ngueguim et al. [9], Hirigoyen et al. [21], Adebayo Ot et al. [22], and Tiogué et al. [23] who highlighted that more than 40% of fsh farmers were over 50 years old. Te high representation of men (93.94%) in fsh farming is in accordance with the fndings of Ngueguim et al. [9], Tiogué et al. [23], and Bouelet Ntsama et al. [24] would be related to the socioeconomic constraints faced by women such as difculties of access to land, lack of capital, poor management skills, and lack of credit opportunities. Te proportion of trained fsh farmers (39.39%) was higher than 5 and 8% reported, respectively, by Tiogué et al. [23] and Hirigoyen et al. [21]. Te reason would be the geographical proximity of the Wouri division with the Institute of Fisheries and Aquatic Sciences (ISH) of the University of Douala at Yabassi whose purpose is to train fsheries engineers. For instance, out of 39.39% of trained farmers, 53.85% came from that higher school. Although the high cost of the biosecurity practice (57.57% of farmers) was the main obstacle, there is no  Veterinary Medicine International  Veterinary Medicine International guarantee that biosecurity measures would be applied even if the cost was low given that farmers do not understand the importance and relevance of the biosecurity practice. Te high percentage (42.42%) of farms in which fsh showed clinical signs of diseases and the low proportion of farms (12.12%) with high productivity (>300 kg/year/m 3 ) would be due to the lack of the biosecurity practice, poor farm management, and lack of fnance. Tough high, the proportion of farms showing clinical signs of fsh infection was below the expected value and likely to increase because of the lack of training in fsh disease diagnosis and the inattention of most farmers claiming not to observe abnormalities in fsh. Te high mortality rate (>15%) of fsh recorded by 66% of the audited farms is probably attributed to the lack of training in fsh farming resulting in the nonobservance of biosecurity measures at the origin of fsh diseases. Te untrained farmers can receive training on biosecurity practices at the Institute of Fisheries and Aquatic Sciences of the University of Douala, Cameroon.
Te overall compliance rate (40.52 ± 14.70%) was intermediate and below the expected high level. In other words, the farms of the Wouri division were of type B or at a moderate risk level of contamination by pathogenic agents, hence the appearance of clinical signs of disease and the high rates of fsh mortality observed in this study. Tis result would be due to fnancial constraints, ignorance, and negligence observed, respectively, in 57.57%, 15.15%, and 9.09% of fsh farmers. Te overall compliance rate is comparable to that reported by Kone et al. [25] and diferent from the low values noted by Obosi and Agbeja [7], Ngueguim et al. [9], Kouam and Moussala [18], Boutin [26], and Ricou [27]. Te reason for this diference would be the increase in the proportion of fsh farmers who have received training and the diference between sociodemographic and technical-economic conditions. Te isolation component was highly and signifcantly the most observed followed by trafc management and sanitation because the measures relating to isolation seem inexpensive and less restrictive. Tis trend is contrary to that outlined by Ngueguim et al. [9], Kouam et al. [19], and Kone et al. [25] as which the most observed component was trafc management followed by isolation and sanitation and which was justifed by the fact that trafc management has few measures compared to the other biosecurity components.
With respect to the frequency distribution of farms according to the compliance rate of biosecurity components, no farm (0%) was at a minor contamination risk level or recorded a high compliance rate (75-100%) of biosecurity components. Tis could be explained by the fact that producers face fnancial constraints, hence the absence of rigorous observance of biosecurity measures. Indeed, this study showed that the fnancing of the biosecurity practice was constraining for 57.57% of fsh farmers. In Cameroon, there is no report on the good biosecurity practice in fsh farms. However, Kouam et al. Visitors not allowed to have contact with water 18 (54.54) 9 No exchange of breeding tools between farms 29 (87.88) 10 Water supply tracks protected to trap debris and unwanted aquatic animals 6 (18.18) Biosecurity component in relation to sanitation 11 Use of footbaths 5 (15.15) 12 Veterinary intervention 0 (0.00) 13 Incineration of dead fsh 0 (0.00) 14 Especial outft (clean coverall and boots) for staf 3 (9.09) 15 Especial outft for visitors 1 (3.03) 16 Analysis of water quality 1 (3.03) 17 Diagnosis Captured fsh put back into water 0 (0.00) 1 : ethological, anatomical, and physiological diagnosis based on skills acquired by farmers during fsh training program attended; n: number of fsh farms. Veterinary Medicine International [19] reported that 9.74% of pig farms had the good biosecurity practice in the West Region of Cameroon and further because that minority of farmers (9.74%) would not have fnancial constraints or would be well trained in pig farming.

Veterinary Medicine International
Te overall adoption rate was intermediate (40.40 ± 30.10%) and varied from 0 to 96.97% due to fnancial constraints and lack of knowledge or training in biosecurity. Indeed, up to 60.61% of fsh farmers in the Wouri division have not been trained in fsh farming. Te most adopted component was isolation followed by trafc control and sanitation because the isolation component would be technically and fnancially less constraining [9,18,19,25]. On the other hand, for same reasons, the latter authors highlighted that trafc control was the most adopted followed by sanitation and isolation. Te least adopted (0%) biosecurity measure were "veterinary visit," "dead fsh incinerated," and "fsh caught not returned to the water," while the most adopted (96.97%) was "breeding infrastructures in derivation." Certain measures are unknown or neglected by fsh farmers or the latter lack fnance to adopt other measures.
Te analysis of the multivariate linear regression of the factors afecting the implementation of biosecurity showed positive and signifcant relationship between the level of education, the health status of the fsh, and the compliance rate of biosecurity measures. A strong, positive, and signifcant relationship between the education level, the herd size, and the level of biosecurity adoption has been reported in beef cattle farms [28]. Ideally, the compliance rate would have negatively afected the health status of the fsh. Hygiene measures would therefore not have the same efectiveness against infectious agents; the most efective would be the most restrictive and the least applied by fsh farmers. Te afnities of the biosecurity practice observed between the farms of certain subdivisions of the Wouri division would refect a sociodemographic and technical-economic rapprochement.
Te issue of compliance with hygiene measures on farms is undeniable because a good practice will allow the ISO  certifcation of farms and will therefore ensure the sanitary quality of fsh and customers. Tis study will certainly help stakeholders in the aquaculture sector in Cameroon and other countries with comparable farming systems to improve the level of the biosecurity risk of farms. Tis will reduce epizootics and optimize production.

. Conclusion
Te present study on the characteristics of fsh farming and biosecurity practices in the division of Wouri, Cameroon, revealed that fsh farming is an income-generating activity that still requires socioeconomic, technical, and institutional eforts for optimal productivity. Overall, the compliance and adoption rates of biosecurity measures were intermediate. No type C farms were recorded. Te compliance rate was signifcantly afected by the age of fsh farmers, the level of education, and training received in fsh farming. Te biosecurity measures to be improved were "veterinary visit," "dead fsh incinerated," and fsh caught not returned to water." A signifcant positive relationship was established between the education level, fsh health status, and biosecurity compliance rate. Biosecurity afnities have been observed between certain farms. Te government should take the issue of aquaculture biosecurity very seriously by emphasizing on the education, training, and capacity building of farmers on biosecurity practices.

Data Availability
Te data used to support the fndings of this study are available upon request to the corresponding author.

Conflicts of Interest
Te authors declare that they have no conficts of interest.