Causes of Anaemia among Women in Fish-Smoking Livelihoods: A Public Health Emergency

Anaemia, defined as an insufficient number of red blood cells in the body, is a major global public health concern which has been linked to morbidity and mortality, low productivity and poor birth outcomes in women (Figueiredo et al., 2018; Mann et al., 2002; Scott et al., 2014).  Well recognized contributors to the high anaemia burden in the African region are iron deficiency due primarily to suboptimal intake of dietary iron, infections and infestations and inherited blood disorders (CDC, 2015).  More recently, chronic inhalation of biomass smoke has also been implicated as a non-dietary risk factor for anaemia among both children and women (Accinelli & Leon-Abarca, 2017; Kyu et al., 2010; Machisa et al., 2013; Mishra & Retherford, 2006; Page et al., 2015). The incomplete burning of biomass fuel produces huge amounts of carbon monoxide (CO), hydrocarbons, oxygenated organics and particulate matter (PM) (Salvi & Brashier, 2014).

The mechanism by which these toxins cause anaemia has not been fully understood. A more probable way biomass smoke has been linked with anaemia is due to its role in triggering systemic inflammation in the body. This systemic inflammation is known to cause anaemia mediated by certain inflammatory cytokines. The cytokines causes anaemia by the dysregulation of iron homeostasis, impaired marrow response to the production of red blood cells and erythropoietin response to reduced haemoglobin (Weiss & Goodnough, 2005)

Over half of people living in developing countries use some form of biomass fuel (e.g. wood, dung, straw and crop residues) for cooking, which is typically done by women (Kyu et al., 2010). Women whose livelihoods expose them to chronic smoke inhalation may be at increased risk of anaemia. Fish smoking using biomass fuel, is an important livelihood for women living in proximity to fishing communities. More than half of women living in coastal areas are involved in fish smoking livelihood (FAO, 2018). The fish smoking industry relies heavily on firewood as a fuel source. Women involved in fish smoking livelihood have additional levels of smoke exposure and associated health consequences including anaemia. A long period of exposure to biomass fuel has been linked to a greater risk of developing anaemia among women of reproductive age (WRA) (Sukhsohale et al., 2013).

Definition of Anaemia

Anaemia is defined as a condition in which the number of erythrocytes or its oxygen-carrying capacity is not sufficient to meet the body’s physiologic needs (WHO, 2011). Anaemia is usually diagnosed when the concentration of haemoglobin in the blood is lower than the set thresholds which are based on the age, sex and physiological status of an individual. According to the World Health Organization, generally, in non-pregnant women of reproductive age (15- 49 years), anaemia is defined as haemoglobin concentration < 8.0g/dL are classified as mild, moderate and severe anaemia respectively among non-pregnant women of reproductive age (WHO, 2011).  The burden of anaemia of a particular country according to the WHO is based on the prevalence rates of the country. Countries with anaemia prevalence of 40% are classified as having a moderate public health problem and a severe public health problem respectively (WHO, 2009).

Prevalence of Anaemia

Anaemia, is a public health problem affecting mainly children and women worldwide. Globally, anaemia affects over 1.62 billion people with the highest prevalence being among children (42.6%). Using nationally representative data from 1995 to 2011, it was reported that, 29.0% and 38.2% of non-pregnant WRA and pregnant WRA were anaemic respectively. Further, anaemia prevalence among non-pregnant WRA ranged from 37.7% to 41.5% in the South-East Asia, Eastern Mediterranean and African regions (WHO, 2015). Although little improvement has been reported for anaemia between 1995 and 2011, its prevalence remains intolerable globally (Stevens et al., 2013).

In 2012, a systematic analysis was conducted from the years 1995 to 2011 to study the trends of anaemia prevalence among pregnant, non-pregnant women of reproductive age and children. Data were gathered about anaemia and haemoglobin concentration for women (15 to 49 years) and children (6-59 months) from 257 population-representative sources from 107 countries around the world. According to the review, globally, anaemia prevalence among non-pregnant women decreased from 33% in 1995 to 29% in 2011. However, the prevalence among high-income countries increased slightly from 14% in 1995 to 16% in 2011 even though the prevalence was still very low as compared to other regions (Stevens et al., 2013).

Most African countries have an anaemia prevalence of severe public health concern. In Africa, anaemia is highly prevalent among children under 5 years, followed by pregnant WRA (WHO, 2011). Anaemia prevalence is highest among pregnant women (56%) and non-pregnant WRA (48%) from Central and West Africa regions. Non-pregnant women in East Africa had the second highest (40%) prevalence of anaemia. During this period, the region with the lowest anaemia prevalence was Southern Africa (33%) (WHO, 2015). Over the years, the anaemia prevalence has improved among non-pregnant women from these regions. In 2011, the prevalence dropped from 52% to 48% in the Central and West Africa region, from 40% to 28% in the East Africa region and also dropped to 28% in the Southern Africa region from 33% (Stevens et al., 2013)

Consequences of Anaemia

Anaemia is known to have negative impacts on the health and wellbeing of, especially women and children. Anaemia increases the risk of premature delivery and low birth weight among women of reproductive age. The increased prevalence of anaemia among women of reproductive age affects performance and work rate. It is also believed to have an effect on pregnancy outcomes in women and the newly born baby, which goes a long way to impact negatively on the health of individuals, economic potential and development of the community. Anaemia due to iron deficiency alone is estimated to cause over 90,000 deaths among both males and females of all age groups. Based on calculations for 10 developing countries, the total economic losses due to reduced work productivity and cognitive losses was almost 17 dollars per capita (Horton & Ross, 2003).

The following are some of the worrisome consequences of anaemia:

  • Maternal and child mortality
  • Decreased cognitive development
  • Low work productivity

Maternal and Child Mortality

Anaemia is linked with increased risk of maternal and child mortality. A meta-analysis of about 12,000 children in six African countries showed that, increasing haemoglobin concentration by 1g/dL decreases the risk of mortality by 24% (Scott et al., 2014). In a systematic analysis to determine the link between maternal anaemia and low birth weight, it was concluded that maternal anaemia was a risk factor for low birth weight (Figueiredo et al., 2018). According to Petrou (2003) preterm birth and low birth weight increase the risk of infants to mortality and morbidity. A research conducted by Muoneke et al. (2012) in Nigeria revealed that out of the 140 severely anaemic children under 5 years recruited for the study, 19 died (a case fatality rate of 13.6%) while 117 (83.6%) recovered. The factors associated with higher mortality among the children in this study were malnutrition (P=0.02), coma (P<0.001), tachycardia (P=0.033) and not receiving blood transfusion (P=0.001). In another study by Khaskheli et al. (2016), the mortality rate of 305 pregnant women with iron deficiency was 5.24%. These women also had an increased risk of having complications such as renal failure (15.73%), and antepartum haemorrhage (16.06%) (Khaskheli et al., 2016).

Decreased Cognitive Development

Evidence suggests that women of reproductive age may be at increased risk of cognitive alterations due to iron deficiency. A blinded, placebo-controlled experiment was performed among women between 18 and 35 years classified as iron sufficient (control group), non-anaemic but with iron deficiency (ID group), or with iron deficiency anaemia (IDA group). Eight (8) cognitive performance tasks (Detterman’s Cognitive Abilities Test) were used to assess the participant’s cognition at baseline (n=149) and after 4 months of the experiment (n=113). The control group performed better on cognitive tasks (p<0.011) and performed them at a faster rate (P<0.038) than the iron-deficient anaemia women at baseline. After treatments, there was a 5 to 7 fold improvement in cognitive performance associated with significant improvement of serum ferritin. Also, there was a positive relationship between the speed at which cognitive tasks were performed and a significant improvement in haemoglobin concentration (Murray-kolb & Beard, 2007).  This study was similar to another research by Sen and Kanani (2006) among adolescent girls in primary school where the non-anaemic girls scored significantly higher in various cognitive function tests even after controlling for undernutrition measured by their BMI. Cognitive development of children may be affected as a result of anaemia. A secondary data analysis conducted on cognition and iron deficiency based mainly on the past 15 years showed that, iron deficiency anaemia has a negative effect on the behaviour, motor skills and cognition of children, with especially those with low socio-economic background more affected (Jáuregui-lobera, 2014). Contrary to Jáuregui-lobera (2014), a study by Akca and Bostanci (2017), to assess the impact of anaemia and body mass index (BMI) on neuromotor development among 916 preschool children revealed that mild anaemia had a positive association on a child’s neuromotor development while being overweight or obese was negatively associated with neuromotor development. However, a major limitation to this study which might have presented a positive effect of anaemia on neuromotor development was due to the fact that children who participated in the study did not show moderate or severe anaemia (Akca & Bostanci, 2017). According to Santos et al. (2009), anaemic children between the ages of two to six years demonstrated poorer language development when compared with children who were not anaemic. This was a cross-sectional study involving 44 children as controls (no anaemia) and 22 as cases (anaemia present). It was observed that there was a significant difference in all the language evaluations between the two groups. The cognition performance score was higher in the controls (77) than the cases (45) at (p<0.001). There was also a significant difference (p<0.02) between the anaemic group (75) and non-anaemic group (100) in terms of the reception performance score (Santos et al., 2009). According to Saloojee and Pettifor (2002) more of the development of the central nervous system (CNS) processes greatly relies on iron-rich enzymes and proteins. This implies that the deficiency of iron may have various effects on brain growth.

Low Work Productivity

Physical working capacity of humans is known to be affected greatly by iron deficiency anaemia. A study conducted by Kalasuramath et al. (2015) showed the effect of anaemia and iron deficiency (ID) on physical and cardiorespiratory fitness of women working in small scale industries in India. The study participants were 600 non-pregnant, non-lactating women (NPNL) who were between the ages of 18 and 55 years. The women were divided into groups of three (200 per group); ID, anaemic and control women. Their physical fitness index (PFI) was determined by using the Queens College step test (QCT) and by calculating the maximum oxygen uptake (VO2 max). The participants with ID had an average VO2 max of 40.24ml/kg/min, women in the anaemic group had an average of 38.65 and the control group had the highest with an average mean of 45.53 ml/kg/min. It was suggested that anaemia and ID both impair the delivery of oxygen to the tissues and thus leads to a reduced VO2 max, therefore, affecting their physical activity levels (Kalasuramath et al., 2015).  Another research was conducted among 30 female students between 16 and 20 years to assess whether iron and energy supplementation improves physical work capacity among them (Mann et al., 2002). The study participants were grouped into two, being anaemic but having adequate energy or being anaemic but having inadequate energy. Both groups were given iron capsules for 9 months to bring their haemoglobin levels to 12 or above. Energy supplements were also given to the energy-deficient group based on the energy gap between the two groups. Exercise time and maximum workload increased significantly (p< 0.01) after iron supplements were given and after both iron-energy supplementation in the two groups (Mann et al., 2002). These results were similar to a study by Sen and Kanani, (2006), which revealed that non-anaemic adolescent girls between 9 and 14 years were able to take more steps and at the same time get back to the recovery time faster than anaemic girls. This was assessed by asking the girls to climb up and down within 3 minutes, a set of five steps. Moderately anaemic girls climbed an average of 165 steps within the three minutes whiles the non-anaemic climbed an average of 175 steps. With regards to the recovery time, anaemic girls took a much longer time 3.69 minutes than non-anaemic girls who took an average of only 2.55 minutes (p<0.001) (Sen & Kanani, 2006).

Causes of Anaemia

Causes of anaemia are multifactorial including both nutritional and non-nutritional factors. Nutritional causes of anaemia mainly comprise nutrient deficiencies arising from poor dietary intake and eating disorders. It is estimated that at least more than half of all anaemia cases around the world may be caused by non-nutritional factors (WHO, 2015). Non-nutritional factors which cause anaemia include conditions such as blood loss from injury or certain physiological states (such as menstruation in women), chronic inflammation, infection and disease as well as drug toxicity (Haidar, 2010).

Nutritional Causes of Anaemia

a. Iron Deficiency Anaemia

Iron-deficiency anaemia is a type of anaemia which is characterised by insufficient iron to produce haemoglobin to carry oxygen to the rest of the body. According to WHO (2015), about 50% of all anaemia cases in the world is believed to be caused by iron deficiency anaemia (IDA). According to a review by Petry et al. (2016), this value is exaggerated, iron deficiency is less than what is assumed. When the results of 25 nationally representative studies which measured ID, IDA and anaemia among children (6-59 months) and women of reproductive age (15-49 years) from all parts of the world between 2003 and 2014 were combined, the proportion of anaemia due to iron deficiency was about 25% among children and 37% among women of reproductive age. For both groups, the proportion of anaemia associated with ID was substantially lower for countries with a severe burden of anaemia (Petry et al., 2016). In the recently ended Ghana Micronutrient Survey in 2017, about 14% of non-pregnant women of reproductive age were iron deficient (GMS, 2017).  Some of the effects of iron deficiency anaemia are characterized by reduced work capacity and cognitive development. Iron supplements have been proven to increase physical activity levels and also improve the cognitive performance of women (Mann et al., 2002; Murray-kolb & Beard, 2007). Signs and symptoms such as easily getting fatigued, weakness, headaches, rapid or irregular heartbeat, brittle nails and dizziness accompany iron deficiency anaemia (Lopez et al., 2016). Women of reproductive age are at increased risk of iron deficiency anaemia due to menstruation, pregnancy and lactation (Jangjoo & Hosseini, 2016). Iron deficiency anaemia during pregnancy is caused by the increased plasma volume (30-40%) compared to the haemoglobin mass and red blood cell volume (20-25%). As a result, there is a reduction in Hb levels, which leads to an increase in the transportation of oxygen to the foetus and the placenta causing an increased demand for iron (Gupta & Gadipudi, 2018).

Not eating enough foods that contain iron also causes iron deficiency anaemia. The bioavailability of iron in foods differs, with haem iron from animal sources proven to be readily absorbed than iron from non-haem sources, typically from plant sources (Killip et al., 2010). A study was conducted by Pasricha et al., (2017) to know how much of an impact meat consumption has on anaemia status among 354 women of reproductive age in Northwest Vietnam. Logistic regression analysis proved that consumption of meat 3 or more times per week was protective against iron deficiency anaemia OR 0.46, p=0.002 (028, 0.76). (Pasricha et al., 2017). The bioavailability of iron in foods can be enhanced or inhibited by different substances as well as cooking methods. Boiling improves iron bioavailability in vegetables. Addition of vitamin C or cooking with vegetables rich in vitamin C such as tomatoes improves the amount of iron available for absorption (Yang & Tsou, 2006). On the other hand, chemical substances such as polyphenols and phytic acid hamper iron bioavailability. Data from the Korean National Health and Nutrition Examination Survey (2007-2012) was used to determine the relationship between green tea, coffee and serum ferritin concentration of Korean adults. Food frequency and 24-hour recall data were used to assess their intake. When multivariate linear regression was used to adjust for age, BMI, educational level, smoking status, physical activity, alcohol consumption, hypertension, diabetes mellitus and daily iron intake, intake of coffee was negatively associated with serum ferritin concentration for both males and females. Serum ferritin levels decreased by 8.4% in males and by 18.8% in females among those who drink three or more cups of coffee in a day (Sung et al., 2018).

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b. Folic Acid and B12 Deficiency Anaemia

Aside from iron deficiency, inadequate folate and vitamin B12 lead to anaemia (Gupta & Gadipudi, 2018). These two vitamins play very crucial roles in many cellular processes in the body. When one or both is not adequate, it leads to a type of anaemia called megaloblastic anaemia (Castellanos-Sinco et al., 2015). Megaloblastic anaemia is due to the impairment of DNA synthesis which is caused by deficiency of folate and vitamin B12. Plasma homocysteine level is used to detect both vitamin B12 and folate deficiency in humans. An advanced effect of megaloblastic anaemia is loss of memory and vision which is characterised by increased serum homocysteine levels (Castellanos-Sinco et al., 2015; Hariz & Bhattacharya, 2019). Megaloblastic anaemia due to vitamin B12 deficiency is referred to as pernicious anaemia. It is mainly caused by either insufficient vitamin B12 from the diet or lack of intrinsic factor which is responsible for its absorption (Lahner & Annibale, 2009). The serum folate, vitamin B12 and homocysteine levels of 50 patients suffering from megaloblastic anaemia were compared with 50 non-megaloblastic anaemia patients (control). A total of 40 (80%) out of the 50 megaloblastic anaemia patients had very low vitamin B12 levels and 44 (88%) had very low folate levels. Out of the 50 control patients, only 2(4%) and 12 (24%) had low vitamin B12 and folate levels respectively. High serum homocysteine level was in 80% of patients expressing low vitamin B12 and folate serum levels (Yadav et al., 2016). Although megaloblastic anaemia is common, research regarding its prevalence around the world is not enough. Its burden is high in countries where malnutrition is a significant problem. The prevalence also increases among the elderly and pregnant women (Hariz & Bhattacharya, 2019). In 2017, the prevalence of megaloblastic anaemia among women of reproductive age (n=22,278) in Pakistan was analysed using the 2011 national-level secondary survey data (Rizvi et al., 2017). An electrochemiluminescence immunoassay method was used to measure serum folate and vitamin B12 levels. The prevalence of vitamin B12 deficiency and folate deficiency among the women was 8,400 (52.4%) and 8,371 (50.8%) respectively. Women who consumed eggs daily and weekly (RR 0.89; 95% CI 0.81, 0.98; P=0.02, and RR 0.88; 95% CI 0.78, 0.99; P=0.03, respectively) were less likely to be suffering from folate deficiency as compared to women who consumed eggs monthly. Increased intake of green leafy vegetables, which are known to be good sources of folate, was also found to lower the risk of folate deficiency anaemia (Rizvi et al., 2017).

Non-Nutritional Causes of Anaemia

a. Infections and Infestations

Diseases or infections can cause anaemia through many mechanisms. Absorption and metabolism could be impaired by infections. Infections may also lead to the onset of anaemia through blood loss, nutritional deficiencies and side effects of medication. Acute and chronic infections like malaria, TB, HIV, cancer and chronic heart failure can all lead to anaemia. (Viana, 2011; World Bank, 2017). For most cases the mechanism by which chronic infections cause anaemia is by the decrease in serum iron, coupled with a decrease in total iron-binding capacity as well as a decrease in the percentage of transferrin saturation due to reticuloendothelial siderosis. Though there may be other mechanisms in play at the same time depending on the type of disease, the main mechanism is the impairment of the reticuloendothelial system. According to Viana (2011), all the processes involved happens due to the brief increase in hepcidin.

b. Soil-transmitted Helminth Infections

Soil-transmitted helminth infections contaminate soil in poor sanitation areas and are usually transmitted by eggs from human faeces. According to WHO (2019a), globally, over 1.5 billion people are affected with soil-transmitted helminth. Roundworm, whipworm and hookworms are the main species that infects approximately over 800 to 1 million, 600 to 800 million and 500 to 700 million people in the world respectively (CDC, 2019; WHO, 2019a). Iron deficiency anaemia, blood and iron loss are caused mainly by hookworm infections. The worms eventually feed on host tissues such as blood which lead to loss of iron and protein. Hookworms may cause anaemia through intestinal chronic blood loss (WHO, 2019a). Hookworm (Ancylostoma duodenale) has been reported to cause a loss of 0.25 mL blood per worm in a day. A hookworm load of about 40 to 160 worms is associated with iron deficiency anaemia based on the iron status of the host. Women of reproductive age and young children are at most risk of developing hookworm related iron deficiency anaemia due to their low levels of iron stores (Shaw & Friedman, 2011).

A study was conducted by Mengist et al., (2017) among pregnant women attending antenatal care to determine the prevalence of anaemia and intestinal helminthic infection in Oromia, Ethiopia. Intestinal helminthic infection was assessed by the collection of single stool specimen and observing it under a microscope. The prevalence of anaemia among the patients was 17.5%. Out of the 372 pregnant women, almost 25% were suffering from intestinal helminths infection. Hookworm infection (15.1%) was recorded as the highest intestinal helminths infection followed by roundworm infection (6.5%). After adjusting for confounders such as residence, age, educational status, food diversity, birth interval and other independent variables, only previous malaria infection within the past year (p=0.003), gestational age (p=0.009), not regularly taking iron (p=0.022) were all significantly associated with anaemia. Also, anaemia was highly prevalent among pregnant women having hookworm infection [AOR, 95% CI: 3.53 (1.6, 6.7), P=0.001] and roundworm infection [AOR, 95% CI: 1.82 (1.1, 3.8), P=0.022] (Mengist et al., 2017). The results from another research by Gopalakrishnan et al, (2018) involving adolescent female school children in an urban area of Tamil Nadu in India confirmed this outcome. Having intestinal parasitic infection among the female students increased the odds of having anaemia by 2.84 times [OR, 95% CI: 2.84 (1.19, 6.76), P=0.014]

c. Malaria

According to the WHO, malaria cases found around the world in the year 2017 was over 219 million leading to approximately 400,000 deaths (WHO, 2019b). A significant number was caused either directly or indirectly by anaemia. About 90% of all malaria cases are from the WHO African Regions and the majority are caused by the Plasmodium falciparum (WHO, 2019b). The prevalence of malaria among pregnant women is 10% and 8.4% in non-pregnant women in Ghana. Over 98% of all the malaria cases was due to the Plasmodium falciparum specie (GMS, 2017). Malaria is known to be one of the important cause of anaemia globally. Pregnant women and children are the most vulnerable, especially in high malaria transmission areas. Malaria-related anaemia involves both decreased red blood cells production and destruction of red blood cells. Its contributions to anaemia depend on other factors such as the age of the person, pregnancy state, genetic make-up of the person affected, antimalarial immune status, and the local endemicity of malaria (White, 2018).  Observational studies involving hospitalized children under five years to estimate the prevalence of malaria parasites and anaemia in Uganda was performed within a year (May 2011 to May 2012) by (Kiggundu et al., 2013). As part of the study blood smears, haemoglobin concentration and HIV testing were done from finger-prick blood samples every 3 months interval. The prevalence of malaria parasitemia and anaemia was 54.6% and 56.3% respectively. The average haemoglobin was significantly (p=0.001) lower in patients with parasitemia (8.3 g/dl) as compared to children with no parasitemia (10.0 g/dl). Again malaria parasitemia was linked with causing 76.8% of all severe anaemia cases among the children (Kiggundu et al., 2013).

d. Genetic Disorders

Anaemia is also caused by several genetic conditions. Genetic blood disorders impacting haemoglobin concentrations, commonly known as haemoglobinopathies, include alpha and beta thalassemia, sickle cell and haemoglobin E. Haemoglobinopathies are a group of inherited disorders characterized by abnormal structure or production of haemoglobin molecule (Kohne, 2011).  Sickle cell disease is characterized by a change in the shape of red blood cell (RBC), unlike a healthy normal RBC which is usually smooth and takes the shape of a donut. Sickled RBCs are not able to pass through the blood vessels. Rather, they cause blockages that deprive other tissues and organs, oxygen-carrying blood (WHO, 2019c). Sickle cell disease is prevalent among people who trace their ancestry to sub-Saharan Africa, regions in the Western Hemisphere, India, Saudi Arabia and some other Mediterranean countries (CDC, 2015; WHO, 2019c). Thalassemia occurs most commonly among people in the Mediterranean, Middle East, Africa and Southern Asia. Thalassemia results when genes controlling for the development of the alpha and beta globin chains are missing or impaired resulting in abnormal haemoglobin with reduced oxygen-carrying capacities. In areas where malaria is endemic, both the alpha and the beta thalassemia are the most prevalent inherited single gene globally (WHO, 2019c). According to Karimi et al. (2015), in females, thalassemia may affect the proper functioning of certain hormones such as the luteinizing hormone, oestrogen, and progesterone leading to delayed puberty and development of secondary sexual characteristics. In a particular study in 2012, anaemia due to genetic haemoglobin disorders was a major predictor of anaemia than iron deficiency (Karakochuk et al., 2015). The aim of the study was to investigate the factors that were associated with anaemia in 450 rural Cambodian women of reproductive age. More than half of the study participants (54%) had a genetic haemoglobin disorder including 25 different gene variants. The two most common genetic haemoglobin disorder affecting them were haemoglobin E trait (14.9%) and thalassemia trait (11.6%) (Karakochuk et al., 2015). The strongest predictors of anaemia were haemoglobin E homozygous disorder 95% CI -18.24 (-21.74, -14.73), P=<0.0001 and pregnancy status 95% CI -11.99 (-15.60, -8.39), P=<0.0001]. The anaemia prevalence among women with genetic haemoglobin disorder was higher (~45%) compared with women without any disorder (~11%) (Karakochuk et al., 2015). Based on a worldwide review by Modell and Darlison (2008), 71% out of 229 countries had haemoglobin disorders present as a significant health problem. Over 300,000 infants are born with haemoglobin disorders from birth with sickle cell anaemia accounting for 83% and thalassaemia accounting for 17%. Over 7% of pregnant women are estimated to be carriers of significant genetic haemoglobin disorders (Modell & Darlison, 2008).

e. Anaemia of Inflammation

Anaemia of inflammation also known as anaemia of chronic disease (ACD) is a type of anaemia that usually occurs in people with chronic disease (e.g. cancer, autoimmune disease, infections) due to inflammation. It is regarded as the second leading cause of anaemia after iron deficiency anaemia globally (Nemeth & Ganz, 2014).  Even though anaemia of inflammation may affect any age group, the elderly are more prone due to the likelihood to develop chronic diseases that cause inflammation. With this type of anaemia, it is possible to have a normal or even increased amount of stored iron in body tissues, but still have a low iron level on your blood (NIH, 2019). The inflammation may prevent the production of healthy RBC’s due to the body losing its ability to use the stored irons which leads to anaemia. Anaemia of chronic disease may occur simultaneously with other conditions, there is no exact cause for it. It may be caused by either decreasing the survival chances of RBCs or the impairment of RBC production or the hormone erythropoietin (NORD, 2018). According to Page et al. (2015) Chronic inflammation is mediated by cytokines which are disruptive in iron homeostasis, reducing the sensitivity of erythropoietin to low haemoglobin levels and also affecting the sensitivity of bone marrow to erythropoietin.

Anaemia, especially in the older population, has been linked with various inflammatory conditions. Recently, a research was conducted among 191 (56 IDA and 135 ACD) consecutively hospitalized geriatric patients with iron deficiency anaemia and anaemia of chronic disease. Out of the patients with ACD, 96 (71%) had acute infections such as respiratory, urinary and gastrointestinal tract infections, 12 (12.3%) were diagnosed with cancer such as prostate, colon cancer, etc. and 22 (16%) were suffering from autoimmune inflammatory diseases such as gout, rheumatoid arthritis and others (Joosten & Lioen, 2015).  Patients with cancer are prone to becoming anaemic due to inflammations. A prospective observational study of 888 cancer patients from 2011 to 2014 showed that the prevalence of anaemia was 63.4% (Macciò et al., 2015).  The authors revealed that the mean haemoglobin concentration varied significantly depending on the type of cancer. For instance, the mean haemoglobin concentration of ovarian cancer patients was the least (10.9 ± 1.8) and it was highest among patients suffering from breast cancer (12.1 ± 0.2). Again, anaemia was more prevalent among patients in advanced stages of cancer (stage 3 to 4). This was further emphasized by the presence of more inflammatory indicators including C-reactive protein (CRP), fibrinogen, interleukin 1 beta (IL-1β), interleukin 6 (IL-6), tumor necrosis factor alpha (TNFα), reactive oxygen species (ROS), erythropoietin among patients in the advanced stage of cancer (Macciò et al., 2015).

Women in Fish Smoking Livelihood

A fairly small number of women are involved in fishing compared to men. Generally, women are known to be actively involved in the post-harvest processing, marketing and distribution of fish (FAO, 2018).  According to the FAO, in 2014, of all people directly involved in the primary sector of fisheries and aquaculture, women accounted for only close to 20%. However, when the secondary sector which involves processing and distribution is added women form about half of the total workforce (FAO, 2018). Among the 243 fish smokers in 9 local markets in Cameroon, it was revealed that all the fish smokers were women and among the married ones, many had husbands who were fishermen and they supplied them with the fish for smoking (Dongmo, 2019). In Africa, women are the dominating force in the large or small scale traditional fish processing and trade in the continent.

In the continent as a whole, different methods such as smoking, drying, frying and salting are used to process, preserve and store fish. However, fish smoking is the most preferred option because of its advantages of prolonging shelf life, enhancing flavour and appearance (Pemberton et al., 2016). Fish smoking is mostly done at the individual or household level. Most fish smokers have been observed to work from their homes and usually prefer to work alone. They often use the help of either their children, other family members or local casual workers (Kwarteng et al., 2016). Some of the major types of fish smoked in the continent are herring, anchovies, salmon and mackerel (Kwarteng et al., 2016; Tall & Failler, 2012). In Africa, there are two seasons which define the availability of fish all year round for smoking (bumper and lean season). Due to replacement of warmer, and nutrient-depleted surface water with cooler and nutrient-rich water (upwelling) in the year, there is a massive increment in the fish catches known as the bumper season. The upwelling is usually greater from June to September and smaller from February to March. The rest of the months are considered as the lean season during which getting fish is quite difficult (Gordon et al., 2011). The fish for smoking are usually purchased from fish traders, however, some of the fish smokers purchase it directly from the fishermen. In the case where enough fish is not available, fish smokers travel to other communities themselves to get more (Gordon et al., 2011).

The process of fish smoking combines cooking, drying and smoking. This combined process employs the use of smoke from firewood, passing it over the fish at a specific temperature (Salvi & Brashier, 2014).  The heat produced cooks the flesh of the fish and eliminates bacteria inside and outside the fish at a temperature of 80ºC. The fish is dried with the heat produced and finally, the fish is smoked by the smoke produced from burning the wood which enhances its shelf life (Kwarteng et al., 2016). The common smoke oven used is the “Chorkor” oven. Through the supply of constant heat from firewood, Chorkor smoker provides uniformly smoked fish. The type and size of fish determine how they are stacked on the racks and prepared (Gordon et al., 2011). The Chorkor smoker came into existence 1969, before the Chorkor smoker, there were other types of ovens namely the cylindrical mud oven, rectangular mud oven, the rectangular metal oven and the Adjetey and Altona ovens. The Chorkor smoker was designed because none of the four types of ovens were able to provide constant intense heat to cook the fish and later dry it over low fire for a long period (Kwarteng et al., 2016). They were not efficient enough to smoke all the catches from the landing site which led to very high post-harvest losses. Aside from producing fish with low market value, the health of the women was also compromised due to the long hours spent on smoking fish (UNDP, 2001). Before the official launch of the Chorker smoker, women who tested it testified that the use of trays made the smoking process easier. Also, it could carry more fish due to the framed wire mesh. Again the trays allowed smoke and heat to be trapped by forming a chimney. Another advantage was that the fish smoked with the Chorkor smoker gained a higher market value (UNDP, 2001).

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Recently a more advanced smoking oven known as the “Ahotor” oven has been developed by the Netherlands Development Organization (SNV). According to the SNV, because the Chorkor and other traditional stoves require a lot of wood, it becomes scares which lead to increase in its prices (SNV, 2019). The Ahotor oven was designed to reduce the wood required to smoke fish. It was also developed to decrease polycyclic aromatic hydrocarbon (PAH) levels and reduce smoke leakages without necessarily decreasing the quantity of fish that can be smoked in a batch (SFMP, 2016). The wood used for smoking fish depends on the geographical location with mangrove, neem, acacia and cocoa trees as the most preferred by many. About

6% of the total cost of processing smoked fish goes into fuelwood with women most at times purchasing them from local wood sellers or trucks from nearby communities (Kwarteng et al., 2016). According to Dongmo (2019), fish smokers based their choices of the use of a particular firewood on the capacity of the wood to heat as the main reason, followed by its ability to colour the fish to make it attractive and its constant availability. Factors such as the cost and proximity to the collection site were not really important.

Use of Biomass Fuel by Women

Globally, over 3 billion people use biomass fuel for their basic needs including cooking, heating and boiling water (WHO, 2006). According to the World Bank (2017), about 81% homes in Africa burn solid fuels, with the majority of them depending on wood-based biomass as their main cooking fuel. In terms of numbers, it is estimated that about 500 million people living in Africa rely on biomass for heating and cooking. This is expected to increase to over 800 million by the end of 2030 (Keles et al., 2017). Wood fuels form about 60% of the total energy used in Ghana. It provides the majority of the energy needed in the informal sectors such as fish smoking, bread baking, traditional textiles, etc. (Energy Commission, 2006).  Among the livelihood activities that predominantly use biofuel is fish smoking, which is important, especially for women living within fishing communities. Women in fish smoking livelihood also play important roles such as cooking and heating in their homes. However, exposure to smoke from biomass fuel varies based on whether cooking or smoking is done indoors or outdoors and based on whether exposure repeats on a regular basis over a long period (Morandi et al., 2009). Women are normally involved in domestic activities as compared to men, which suggest that they are more exposed to smoke from biomass fuel (Piddock et al., 2014). Because females mostly do the cooking in many households around the world, they are largely in the collection of fuel as well (Cecelski & Matinga, 2014). Therefore, in addition to their constant inhalation of biomass fuel smoke, females are also faced with other associated health and social issues associated with collecting biomass (AFDB, 2016). Urban populations have access to cleaner fuels than rural populations where cost and infrastructure hinder them from the use of clean efficient fuels. In a study in some rural areas in India conducted by Attimogge and Devi, (2014) to assess the reasons why people use a particular type of biomass fuel, almost 90% of the people preferred using firewood due primarily to its low cost. The type of fuel used in a particular household may also depend on the educational level. Lower educational attainment corresponded to greater use of wood and less use of electricity in a cross-sectional study of household biomass fuel in Malawi (Piddock et al., 2014). Biomass fuel combustion produces many pollutants which could be harmful to the body. Some women are not even aware of the risks involved with the constant exposure to biomass smoke. Over 200 chemicals have been discovered in wood smoke and more than 90% of these chemicals are in inhalable range. Normally, women and children inhale an excessive amount of smoke day in day out which is equivalent to two packs of cigarettes in a day (WHO, 2006). According to Kamal et al. (2015), two packs of cigarette forms a total of 40 mg/m3 suspended particles, whiles the total suspended particles emitted from biomass smoke is approximately 10,000 mg/m3, an amount which is higher in many folds. Some of the significant substances in biomass fuel smoke are particulate matter (PM2.5), carbon monoxide (CO), sulphur dioxide, nitrogen dioxide, aldehydes, free radicals and polycyclic aromatic hydrocarbons (PAHs) (Machisa et al., 2013). Even though not enough research has been done, it has to an extent been proven that these compounds from biomass fuel combustion are linked to anaemia (Kyu et al., 2010; Machisa et al., 2013; Honda et al, 2017, Kamal et al, 2015). Chronic inhalation of smoke from the incomplete burning of biomass fuel through cooking and boiling has also been linked with lung cancer (Bruce et al., 2015). Comparing the old traditional “Chorkor” oven to the more improved smoker “Ahotor” oven, it was observed that carbon monoxide and PM2.5 were reduced by 12% and 13% respectively in the Ahotor oven, compared to the Chorkor oven (SFMP, 2016). Again the PAH analysis revealed that the Chorkor oven produced benzo[a]pyrene (BaP) and PAH4 of 22 μg/kg and 84 μg/kg respectively as compared with the 5.9 μg/kg (BaP) and 53.1 μg/kg (PAH4) produced by the Ahotor oven. The increased level of PAH in the Chorker oven is mainly due to the absence of a fat collecting system, which prevents fats, blood and other fluids from the fish from dripping into the fire to burn (SFMP, 2016). Research has shown that women who smoke fish have increased risk of respiratory illness and reduced pulmonary function (Dienye et al., 2016; Torres-Duque et al., 2008).  A case-control study among women 15 years and above involved in fish smoking in Nigeria was conducted. The study aimed at determining the prevalence of respiratory symptoms and also to assess the lung function of women fish smokers and non-fish smokers. The prevalence of all respiratory symptoms parameters measured during the study including sneezing (153; 72.86%), catarrh (159; 75.71%), cough (138; 65.71%) and chest pain (59; 28.1%) were all significantly higher among fish smokers compared with the non-fish smokers, odds ratio (OR) 2.49, 95% CI (1.62,3.82), P<0.001, OR 3.77,95% CI (2.44,585), P<0.001, OR 3.38, 95% CI (2.22,5.15), P<0.001 and 6.45,95% CI (3.22,13.15), P<0.001, respectively . The lung function which was assessed by recording the peak expiratory flow rate (PEFR) showed that fish smokers had a lowered average PEFR (321 ± 58.9+3 L/min) as compared to the non-fish smokers (400 ± 42.92 L/min)(Dienye et al., 2016) .

Mechanisms of Biomass Fuel Exposure and Anaemia

The link between exposure to biomass fuel smoke and anaemia in women and children is not widely known. It is believed that, as chemical substances from biomass fuel smoke enter the human body, it affects the haemoglobin formation process (Raub et al., 2000). According to Murray (2007), carbon monoxide a gas produced from the incomplete combustion of biomass fuel is able to bind more rapidly to haemoglobin than oxygen. When CO binds with haemoglobin it forms a compound called carboxyhaemoglobin (HbCO) which can decrease the amount of haemoglobin available for oxygen-transport and also decrease oxygen carrying capacity of haemoglobin (Fielding, Lang, & White, 2001; Prockop & Chichkova, 2007). Also, particulate matter (PM2.5), a compound from biomass fuel combustion has been shown to increase systemic inflammation and impact bone stimulation negatively (Cliff et al., 2016; Dabass et al., 2016; Page et al., 2015). Systemic inflammation leads to decreased haemoglobin or erythrocytes production and eventually anaemia by downregulation of erythropoietin production or continuous upregulation of hepcidin (Honda et al., 2017). In a study to determine the association of particulate matter (PM2.5) and nitrogen dioxide (NO2) on haemoglobin concentrations and anaemia prevalence, increase in both PM2.5 and NO2 were significantly associated with lowered haemoglobin concentration and increased prevalence of anaemia (Honda et al., 2017).

Polycyclic Aromatic Hydrocarbons (PAHs) from smoke emission is associated with anaemia (Kamal et al., 2015). PAHs has been found to induce oxidative stress that affects erythrocytes. Due to the formation of Heinz body caused by the attack of PAH metabolites on haemoglobin, there is a change in the morphology of RBC and its ability to carry oxygen throughout the body. Finally, the erythrocytes go through a process called cell lyses which leads to a leakage of haemoglobin (Kamal et al., 2015).

Evidence of the Association between Biomass Fuel Smoke Exposure and Anaemia

Women are mostly involved in cooking and most of the time, their children are with them during the process. Exposure to smoke from biomass fuel has been linked to various health implications such as stunted growth (Mishra & Retherford, 2006), increased risk of respiratory disease Mishra (2003) and low birth weight Boy et al. (2002) among women and children.  Biomass smoke exposure may also be associated with anaemia among children. Few published studies have assessed the impact of exposure to biomass fuel on anaemia status of children (Accinelli & Leon-Abarca, 2017; Kyu et al., 2010; Machisa et al., 2013; Mishra & Retherford, 2006). An earlier research conducted by Mishra & Retherford (2006) suggests that the use of biomass fuel only for cooking and heating exposes children to moderate to severe anaemia. The study was based on the 1998-1999 national survey in India of over 29,000 children under 3 years. Weight, length/height were measured, haemoglobin concentration as well as their exposure to smoke based on the type of fuel used in their households for cooking and heating. About 50% of the children from households which use only biofuels such as wood and crop residues had a moderate to severe anaemia. The relative risk of moderate to severe anaemia was still significantly higher in children from households using biofuels only [RRR, 95% CI: 1.58 (1.28,1.94) P<0.001] than children who lived in households using only cleaner fuels after controlling for various confounders. This result was very similar to a much wider study by Kyu et al. (2010) where data on children under five years of age were gathered from the Demographic and Health Surveys of 29 developing countries between 2003 and 2007. The household use of biomass fuel per country level was used to categorize countries into high, moderate and low exposure level. Using multinomial logistic regression, moderate exposure and high exposure to biomass fuel smoke increased the odds of moderate to severe anaemia by 2.36 (OR, 95% CI 1.24, 4.36) and 2.80 (OR, 95% CI 1.37, 5.72) respectively (Kyu et al., 2010).

In a more recent study by Accinelli and Leon-Abarca (2017), the association of solid fuel use and anaemia among children under 5 years from 193 countries was assessed. Countries with higher biomass fuel use had a greater incidence of anaemia (Correlation=0.749, P<0.0001). The authors suggest that exposure to biomass fuel smoke is a significant independent predictor of anaemia (P-value=0.012) when the prevalence of measles immunization, anaemia in pregnant mothers, tobacco smoking, girls primary education and life expectancy were controlled (Accinelli & Leon-Abarca, 2017). Contrary to the three studies discussed above, there was no significant association observed between household biomass fuel use and anaemia among children (6-36 months) according to (Machisa et al., 2013). Data for the study were generated from the 2006-2007 Swaziland Demographic Survey. A major limitation to the study which could have underestimated the association between biomass fuel use and anaemia was the failure to assess exposure to biomass fuel smoke other than cooking. They argued that during winter, for example, it is a common habit for households to use biomass fuel for heating even for longer hours than cooking (Machisa et al., 2013)

Though very limited, anaemia has been linked with biomass fuel use among women of reproductive age. Page et al. (2015) proposed that chronic inhalation of smoke from biomass fuel contributes to anaemia in pregnant women. This study was based on a secondary analysis of data from the Maternal and Newborn Health Registry Study among 12,782 pregnant women in Nagpur, India. More than half (56%) of the study participants reportedly used biomass fuel while the remaining participants used cleaner fuel (44%). Anaemia was significantly higher in women who lived in households using biomass fuel as compared to women living in households using cleaner fuels (93% vs 88%: P<0.0001). Using multinomial logistic regression to control for age, educational level, BMI, household tobacco smoke exposure, trimester, parity, and prenatal iron and folate supplements among the women (Page et al., 2015). The adjusted relative risk of mild anaemia among women living in households using biomass fuel was 1.38 (95% CI: 1.19, 1.61) times greater than women using clean fuels. Moderate to severe anaemia was also 1.79 (95% CI: 1.53, 2.09) times greater in biofuel users than non-biofuel users (Page et al., 2015). A study was conducted in rural Nagpur in India to assess if anaemia and other morbidities were associated with the use of various types of cooking fuels among non-pregnant, non-smoking women of reproductive age (Sukhsohale et al., 2013). The exposure index (EI) of the women was assessed by multiplying the average number of years spent cooking and average hours spent cooking in a day. A total of 360 women had a low (EI<50), 222 had moderate exposure (EI=50-100) and 178 women had a high exposure index (EI≥100). Women with the highest exposure index were more anaemic 53 (29.8%) compared to moderate exposure 46 (20.7%) and low exposure 46 (12.8%) at a P<0.001 (Sukhsohale et al., 2013)

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