Lancet Diabetes Endocrinol Diabetes and Hypertension

638 www.thelancet.com/diabetes-endocrinology Vol 7 August 2019
Lancet Diabetes Endocrinol
2019; 7: 638–47
Published Online
March 13, 2019
http://dx.doi.org/10.1016/
S2213-8587(19)30082-8
See Comment page 590
See Series page 648
This is the first in a Series of
two papers about diabetes in
humanitarian crises
Division of Endocrinology,
Diabetes and Hypertension,
Brigham and Women’s
Hospital, Boston, MA, USA
(S Kehlenbrink MD);Health in
Humanitarian Crises Centre
(J Smith MBBS) and Centre for
Global Chronic Conditions
(E Ansbro MSc, D C Fuhr PhD,
A Cheung BHSc, P Perel PhD,
B Roberts PhD), London School
of Hygiene & Tropical Medicine,
London, UK; International
Rescue Committee, New York,
NY, USA (R Ratnayake MHS);
Médecins Sans Frontières,
Geneva, Switzerland
(P Boulle MPH); and Médecins
Sans Frontières, London, UK
(K Jobanputra MPH)
Correspondence to:
Dr Sylvia Kehlenbrink, Division of
Endocrinology, Diabetes and
Hypertension, Brigham and
Women’s Hospital, Boston,
MA 02115, USA
[email protected]
edu
Diabetes in humanitarian crises 1
The burden of diabetes and use of diabetes care in
humanitarian crises in low-income and middle-income
countries
Sylvia Kehlenbrink, James Smith, Éimhín Ansbro, Daniela C Fuhr,Anson Cheung, Ruwan Ratnayake, Philippa Boulle, Kiran Jobanputra,
Pablo Perel, Bayard Roberts
Human suffering as a result of natural disasters or conflict includes death and disability from non-communicable
diseases, including diabetes, which have largely been neglected in humanitarian crises. The objectives of this Series
paper were to examine the evidence on the burden of diabetes, use of health services, and access to care for people with
diabetes among populations affected by humanitarian crises in low-income and middle-income countries, and to
identify research gaps for future studies. We reviewed the scientific literature on this topic published between 1992 and
2018. The results emphasise that the burden of diabetes in humanitarian settings is not being captured, clinical guidance
is insufficient, and diabetes is not being adequately addressed. Crisis-affected populations with diabetes face enormous
constraints accessing care, mainly because of high medical costs. Further research is needed to characterise the
epidemiology of diabetes in humanitarian settings and to develop simplified, cost-effective models of care to improve
the delivery of diabetes care during humanitarian crises.
Introduction
Forced migration due to conflict has reached a record
number with 68·5 million people forcibly displaced
from their homes by the end of 2017.1
Of these people,
25·4 million refugees have fled across international
borders and approximately 40 million people have been
forcibly displaced within their own country.2,3
Approximately 100 million additional people are affected
by conflict, but are not displaced.4
Natural disasters affect
an estimated 175 million people annually.5
Additionally,
humanitarian crises are increasingly becoming
protracted with an average length of forced displacement
of more than 20 years.3
Low-income and middle-income
countries (LMICs) host around 84% of forced migrants
globally and commonly have very limited resources to
respond to their health needs.3
LMICs also have the
largest burden of diabetes.
Individuals with diabetes are particularly vulnerable
in humanitarian crises, given the disruption of health
services, impeded access to food supplies because of
insecurity, and population movement.6
These factors
increase the risk of exacerbation of medical complications
associated with diabetes, particularly for those with
type 1 diabetes. Additionally, crisis-affected populations are
at risk of diabetes development or exacerbation diabetes
secondary to mental disorders and risky behaviours, such
as harmful alcohol use. The increasing trend towards the
urbanisation of crisis-affected populations might also
implicate environmental risk factors associated with diet,
physical activity, and tobacco use.7
Moreover, childhood
malnutrition and exposure to maternal undernutrition in
utero increase the risk of diabetes in adulthood.8,9
The issue of diabetes and other non-communicable
diseases (NCDs) has largely been neglected in humanitarian
settings.6,10–12 Historically, the main causes of morbidity and
mortality in humanitarian settings were infectious diseases
and malnutrition, particularly among children.12 Given
global epidemiological changes and the fact that LMICs
(where the underlying burden of NCDs is high) are now
commonly affected by crises, humanitarian agencies and
governments are challenged with how to effectively address
diabetes and other NCDs.6
Although published literature
on the burden of NCDs in LMICs is increasing, including
on diabetes, it is unclear whether these studies can be
generalised to humanitarian contexts. Although the Global
Burden of Disease study 201713 provides some background
information on disease burden (including diabetes) in
crisis-affected countries, the data are not accurately updated
to reflect changed disease profiles during crises.
Additionally, it does not capture disease burden data
specifically among populations affected by humanitarian
crises (eg, refugees, internally displaced people, or those
entrapped in conflict-affected areas). Moreover, the burden
of diabetes and the interventions that are most effective and
feasible are unknown, and no evidence-based guidelines or
basic diagnostic, clinical, and preventive resources for the
management of diabetes in humanitarian contexts are
available.10,11
This Series seeks to outline the evidence on the burden
of diabetes among crisis-affected populations and capture
contemporary challenges in the management of diabetes
in humanitarian crises in LMICs. The aims of this first
Series paper are to examine the evidence on the burden
of diabetes among populations affected by humanitarian
crises in LMICs; describe the evidence on health service
use and access to care for people with diabetes in these
settings, to identify main research gaps; and propose
Series
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priorities for future research. The second Series paper
describes the concrete challenges of diabetes care
delivery in humanitarian crises.14
Existing evidence
We identified evidence from 41 eligible studies.15–55 All
studies were published between 1992 and 2018, with
33 published since 2011. 38 studies reported on populations affected by armed conflict,15–23,25–31,33,34,36–55 two on
populations affected by natural disasters,32,35 and one on
all crisis types.24 34 studies were done in the protracted
crisis phase (crisis duration longer than 6 months),15–23,25–31,
33,37–46,48,50–55 three in the emergency response phase
(immediate aftermath of the event up to 6 months),34,47,49
two in the early recovery phase (more stable period of
rebuilding up to 2 years following the crisis),32,36 and
two reported on multiple crises phases.24,35 25 studies
addressed refugee populations,15–19,23,24,27–29,31,33,37–41,45,46,48,50–53,55
five addressed internally displaced people,20,26,30,44,54 and
11 addressed non-displaced conflict-affected popula
tions.21,22,25,32,34–36,42,43,47,49 The majority of studies were done in
the WHO eastern Mediterranean (n=30),15–22,26–31,37–42,44–
46,48,50–55 followed by Europe (n=6),23,25,34,43,47,49 western Pacific
(n=2),32,35 southeast Asia (n=1), and Africa (n=1), and one
study investigated refugees bound for the USA.24 Further
details on the studies can be found in the panel and in
the appendix.
Burden of diabetes
The evidence on the burden of diabetes among crisisaffected populations was extremely scarce and the overall
quality of the studies was poor. Diabetes was most
commonly used as a single diagnosis, and distinctions
between type 1 diabetes, type 2 diabetes, and gestational
diabetes were rarely made. Three studies focused
exclusively on type 1 diabetes;25,47,49 eight categorised
patients into type 1 diabetes, type 2 diabetes, or
both;22,30,31,38,39,45,50,51 and two reported on women with
gestational diabetes.19,33 Atypical forms of diabetes were
not addressed. Only 18 studies15,16,18–21,23,26–29,31,43,44,48,50,53,54
assessed the burden of diabetes at the population level by
the use of probabilistic sampling (rather than healthfacility level with non-probabilistic sampling) and the
majority of these studies relied on self-reporting rather
than medical diagnosis.
Diabetes prevalence varied substantially between
studies examining conflict-affected populations within
the same region. Prevalence of diabetes in displaced
Syrian populations during the crisis ranged from as low
as 0·8% in Syria54 in 2015 and Iraq51 in 2016 to as high as
35% in certain governorates of Iraq.15 When examining
older populations (age >60 years), diabetes prevalence
ranged from 31·8% in Syria29 to 47% in Lebanon.53 An
assessment on the health-care needs of internally
displaced populations in Iraq reported a 2·8% prevalence
of gestational diabetes.20 However, over half of the
pregnant women interviewed had not received a single
antenatal visit by their third trimester and, therefore, had
not been screened for gestational diabetes.
In Europe, two studies reported pre-conflict and postconflict incidence of insulin-dependent diabetes in
Croatia by the use of the national diabetes registry.47,49
One study reported the annual age-adjusted incidence of
this disease in children (ages 0–15 years), in Zagreb,
of 7·0 per 100 000 population (95% CI 3·8–11·8) in 1988
(before the war) and 7·8 (4·5–12·5) in 1991 (after
the war).47 The second study reported an annual
incidence of insulin-dependent diabetes in Zagreb of
6·6 per 100 000 population (any age) in 1988 and 5·9 per
100000 population in 1992.49 In the Tuzla region of
Bosnia and Herzegovina, which was severely affected by
war (1992–95), the incidence of non-insulin dependent
diabetes from 1990 to 1998 was difficult to obtain because
of the war and was assumed to be 3·03 per 100000 personyears, compared with neighbouring Slovenia during that
same period, where the incidence was 8·54 per
100000 population.25 In Turkey, 4·1% of Syrian refugees
self-reported a diagnosis of high blood sugar (not further
defined) in the previous 12 months.23
The only study done in southeast Asia reported the
prevalence of gestational diabetes in a refugee camp at the
Thailand–Myanmar border, based on screening pregnant
women with a 75 mg oral glucose tolerance test.33 Although
the sample size was small (n=228) and the number of all
Panel: Key study characteristics
Study population
Refugees (n=25);15–19,23,24,27–29,31,33,37–41,45,46,48,50–53,55 internally displaced people (n=5);20,26,30,44,54
other conflict-affected populations (n=11);21,22,25,32,34–36,42,43,47,49 affected by natural
disasters (n=2)32,35
Study location
Eastern Mediterranean (n=30);15–22,26–31,37–42,44–46,48,50–55 Europe (n=6);23,25,34,43,47,49 western Pacific
(n=2);32,35 southeast Asia (n=1);33 Africa (n=1);36 multiple regions (n=1)24
Study design
Cross-sectional survey (n=37);15–24,26–33,36–42,44–55 retrospective cohort study (n=2);25,43 prospective
cohort study (n=2);34,35 routine clinical or organisational data (n=14)24,30,36–42,45–47,49,55
Outcome measure
Diabetes diagnostic criteria: self-reported diagnoses (n=12),18–21,23,26–29,34,44,53 fasting capillary
glucose (n=5),38–41,52 random capillary glucose (n=1),48 diabetes criteria not specified
(n=15),15–17,24,25,30,35–37,42,45,46,49,54,55 oral glucose tolerance test (n=1),33 WHO diagnostic criteria
(n=1),31 American Diabetes Association diagnostic criteria (n=1),22 HbA1c (n=5);32,43,47,50,51
diabetes complications (n=5);28,38,39,50,51 glycaemic control (n=7);22,38,39,43,47,50,51 cardiovascular
risk control (n=6)22,38,39,43,50,51
Diabetes type
Type 1 diabetes (n=10);25,31,38,39,45,47,49–51,55 type 2 diabetes (n=13),22,30,31,38,39,43–45,47,50–52,55 gestational
diabetes (n=2),20,33 type of diabetes not specified (n=24)15–19,21,23,24,26–29,32,34–37,40–42,46,48,53,54
Barriers in non-communicable diseases health-service access
Cost (n=10),15,16,18–20,26–29,53 lack of available services (n=5),15,16,19,26,29 geography or did not
know where to go (n=6)15,16,18,20,26,28,29,53
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pregnant patients in the catchment area was not recorded,
the estimated prevalence was 10·1% using Hyperglycaemia
and Adverse Pregnancy Outcomes trial cutoff values.56
In Africa, the only identified study was a retrospective
study evaluating mortality patterns based on chart review
at a hospital in Liberia.36 2% of deaths from January to
July, 2005, were attributed to diabetes.
Glycaemic control and diabetes complications
Seven studies reported on glycaemic control,22,38,39,43,47,50,51
but how this was assessed varied and often relied on
fingerstick glucose readings at different times of day,
such as fasting or 2 h postprandial glucose, so study
comparison is difficult. HbA1c measurements were
reported in six studies.22,25,43,47,50,51
An analysis of the national diabetes registry in
Croatia during the war in 1991 reported a median fasting
glucose of 194·4 mg/dL (IQR 66·7) in displaced people
(mean HbA1c 9·8% [SD 8·7–11·5]) and 183·6 mg/dL
(52·2 mg/dL) in non-displaced people (9·1% [8·0–10·7]),
which was not signif­icantly different (p=0·38).47 In
Bosnia and Herzegovina, a study assessed the effect of
3 years of war on glycaemic control with hospital data
from Sarajevo. Between 1992 and 1994–95 a mean
weight-loss of 11·7 kg (SD 8·2 kg) was measured with a
reduction in mean fasting glucose from 207·0 mg/dL
(SD 54·1) pre-war to 176·4 mg/dL (61·3) post-war, and
HbA1c reduction from 10·3% (SD 2·4) to 9·0% (2·0;
p<0·01).43 These changes were accompanied by a
reduction in blood pressure and hypoglycaemic
medication use.
In the eastern Mediterranean, a cross-sectional study of
Syrian refugees in a camp setting in Iraq reported a
mean HbA1c of 9·3% (SD 1·9) in individuals with type 1
diabetes (16 [5%] of 328 patients).51 Of these patients,
9·1% had HbA1c of less than 7·5% (<58 mmol/mol) and
81·8% of more than 8·0% (>64 mmol/mol). Among
those with type 2 diabetes (312 [95%] of 328 patients), the
average HbA1c was 8·8% (SD 1·7%), with 4·7% having an
HbA1c of less than 7·5% and 62% more than 8%.
Two studies by the UN Relief and Works Agency for
Palestine Refugees (UNRWA) assessed glycaemic control
with 2 h postprandial glucose test in Palestinian refugees
in Jordan.38,39 In one study, 836 (42%) of 2851 refugees
with diabetes attending the clinic had their postprandial
glucose measured.39 Of these patients, 50% had a 2 h
postprandial glucose of less than 180 mg/dL, which was
considered good control. In the second study, done 1 year
later, 99% of those attending the clinic (n=9691) had their
postprandial glucose measured, of whom 65% had a
reading of less than 180 mg/dL.38 The authors suggested
that their eHealth system, introduced in 2012, might
have had incomplete recording and documentation at the
time. A year later, the documentation had improved and
the eHealth system seemed to be working better, which
might explain the differences in the readings between
the two studies.In Yemen, a significant increase (p<0·001
in HbA1c from 7·7% (SD 1·9) to 9·4% (2·4) was identified
when comparing the same individuals before and during
the war.22
Diabetes complications and surveillance were mentioned
in five studies.31,38,39,50,51 In two studies by UNRWA in Jordan,
the most common complications noted were myocardial
infarction, congestive heart failure, and stroke.38,39 Another
study by UNRWA of Palestinian refugees in Gaza Strip,
Jordan, Lebanon, and the West Bank reported that the
most common complications were peripheral neuropathy
(52·6%), foot infections (17%), diabetic retinopathy (11%),
and myocardial infarction (9·6%).50
Among Syrian refugees in a camp setting in Iraq,
63·6% of individuals with type 1 diabetes self-reported
episodes of symptomatic hypoglycaemia, and 36·6% reported at least one episode of diabetic ketoacidosis.51
Among those with type 2 diabetes, 24·3% reported at least
one episode of hypoglycaemia and less than 1% reported
at least one episode of diabetic ketoacidosis. Hyperosmolar
hyperglycaemic syndrome was not reported.
Cardiovascular risk
The control of cardiovascular risk factors in populations with diabetes, particularly hypertension and
hyperlipidaemia, was addressed in six studies.22,38,39,43,50,51
Two studies compared hypertension control in cohorts of
individuals with type 2 diabetes before and after the
conflict. In Yemen, blood pressure control in the cohort
with diabetes improved after the war.22 Likewise, in a
cohort of 55 individuals with insulin-dependent diabetes
in Sarajevo, 25 had blood pressure readings of more than
140/90 mm Hg before the war compared with only
14 people after the war (p<0·01).43
Three studies that reported on cardiovascular risk in
populations with diabetes were based on surveys of
UNRWA programmes for Palestine refugees mostly
collected via eHealth records. The first study50 was a
survey of UNRWA health centres in 2011 and reported
the presence of comorbid hypertension in 68·9% of the
population with diabetes. 55·5% of patients had blood
pressure readings of 140/90 mm Hg or less and 28·2%
had readings of 130/80 mm Hg or less; the remaining
patients had blood pressure readings of more than 140/90
mm Hg. Cholesterol was elevated (>200 mg/dL) in 39·8%
of the population. Only 53·4% of patients with
hyperlipidaemia were on lipid-lowering drugs and most
were making out-of-pocket payments.
A second study39 with Palestine refugees in Amman,
Jordan, showed that 79% of the population had an
associated diagnosis of hypertension, of whom 63% had
their blood pressure measured, with 75% of these patients
having readings of less than 140/90 mm Hg. For
evaluations during the previous 12–15 months, all patients
with diabetes were reported to have had total cholesterol
measured and 72% had cholesterol of less than 200 mg/dL.
The third study evaluated cumulative and quarterly data on
diabetes treatment outcomes from primary health-care
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clinics across Jordan.38 The authors reported that 78% of
patients returned to the clinic within the previous quarter
with more than 99% having their blood pressure and
cholesterol assessed. Of these patients, 82% had a blood
pressure of less than 140/90 mm Hg and 71% had
blood cholesterol less than 200 mg/dL. These three studies
by UNRWA document high prevalence of cardiovascular
risk factors among individuals with diabetes and show the
ability of eHealth records to track and monitor these
comorbidities in protracted refugee situations.
Among Syrian refugees with diabetes in a camp in
Iraq, 9·1% with type 1 diabetes and 55·4% with
type 2 diabetes were on antihypertensive drugs (67·3%
on angiotensin-converting enzyme inhibitors).51 Systolic
blood pressure was controlled in 81·8% of refugees with
type 1 diabetes and diastolic blood pressure in 72·6% of
these patients. Regarding patients with type 2 diabetes,
systolic blood pressure was controlled in 54·9% of
patients and diastolic blood pressure in 36·3% of patients.
9·1% of refugees with type 1 diabetes and 49·7% of those
with type 2 diabetes were treated with statins. However,
in both groups, cholesterol was not significantly different
between those on and off statins.
Health service use and access to care
Ten studies reported health service use (the frequency
and type of care consumed) and access to care,15,16,18–20,26–29,53
of which seven reported data on NCDs as a group (all
included diabetes) and three studies reported data on
diabetes separately.20,27,28 All were cross-sectional household surveys done in the eastern Mediterranean, which
limits the generalisability of the findings. Care-seeking
behaviours, access to care, and health service use were
generally not defined, making the results difficult to
interpret. None of these studies reported data on health
service use or access to care disaggregated by gender.
Although health-care service use was mostly reported for
NCDs as a group, the results are described in this Series
paper because they include information on access to care
for people with diabetes, and the barriers to care for
different NCDs are often similar.
Care-seeking behaviours for those with self-reported
NCDs who needed care were generally high among
displaced populations in urban and camp settings in the
eastern Mediterranean (these were the only studies that
included such data).18,19,28,29 Care was most commonly
sought in primary health-care facilities.18,19,27 One study
reported that refugees with self-reported diabetes had the
highest frequency of care-seeking among Syrian refugees
with an NCD in Lebanon;27 88·2% of Syrian refugees with
diabetes had sought care since their arrival and 70% within
the 3 months preceding the survey (of whom
60·8% sought care in primary health-care centres).
Among displaced Yazidis in Iraq, 92·9% of those
reporting an NCD diagnosis had seen a health provider
for their condition during the 3 months preceding the
survey.26 In Jordan and Syria, 85% of Iraqi refugees
indicated that medical attention was sought the last time
it was needed.29
Despite high proportions of care-seeking behaviour,
access to health services and medicines for NCDs
appeared limited. Among Iraqi refugees with NCDs in
Jordan and Syria who reported a high proportion of careseeking behaviour (>80%), only 62·5% of those in Jordan
and 58·8% of those in Syria could access medical care
when necessary.29 In Lebanon, 56·1% of Syrian refugees
reported difficulty accessing care for NCDs.18 Among
older Syrian refugees (>60 years of age) in Lebanon, of
whom 47% reported having diabetes, nearly all surveyed
reported an inability to obtain adequate medical
treatment, primarily because of cost (3% reported having
the resources to afford medications).53
High costs because of out-of-pocket payments for
consultation fees, medication prices, diagnostic tests,
and transportation were the most common reason for
not being able to access or continue care among all NCDs
in all ten studies.15,16,18–20,26–29,53 High costs were prohibitive
to care-seeking for over half of Syrian refugees with
diabetes in Jordan (51·7%).28 In Lebanon, 91·2% of
Syrian refugees reported the expense of medical services
as the greatest obstacle when seeking care for NCDs.19 In
the same study, 46·1% of people with chronic conditions
reported treatment interruptions, primarily because of
medication costs (89·3%), whereas 6% interrupted
treatment because of danger in the area where
medications were disbursed. Among Yazidis with NCDs
displaced in Iraq who had reported high proportions of
care-seeking behaviour, 40·0% were not taking
prescribed medications, mainly citing the high costs.26 In
Lebanon, 31·5% of Iraqi refugees with chronic conditions
were not taking medications because of the cost (78·9%)
or lack of availability (10%).19
Approximately 70% of all Syrian refugees in Lebanon
paid out-of-pocket for consultant, diagnostic, and laboratory fees.27 The authors of the study noted that refugee
spending on consultation fees was similar among
the five NCDs assessed in the study, when measured
by the proportion of patients with an out-of-pocket
consultation payment.27 A UN High Commissioner for
Refugees (UNHCR) survey estimated that the average
monthly out-of-pocket general health expenditure was
US$90 per household for Syrian refugees in Lebanon who
needed care (the average monthly non-assisted household
income was $173).18 Another survey reported a mean
monthly expenditure on health for Iraqi refugees of $70 in
Jordan and $91 in Syria.29 Most of the expenses were at
outpatient and inpatient facilities for services and
treatment (52·5%), and medicine and treatment supplies
(29·0%). To cover these costs, 53·9% of Syrian refugees in
Lebanon borrowed money, 39·4% used household income,
and 27·8% relied on relatives or friends.18
Aside from the cost of care, the unavailability of health
services, and diabetes care specifically, were barriers to
care.15,19,20,33 In a study of Iraqi internally displaced people,
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the lack of medication at health facilities was cited as the
most important barrier (23·7%).20 Only six papers in the
literature review mentioned the types of diabetes
medications that were prescribed and none reported on
their availability.22,31,41,42,50,51 The next most common barrier
to access was a lack of services (18·4%). A report on
Syrian refugees in Iraq cited the unavailability of services
and the cost of care as the most common challenges
of accessing health care.15 In two districts in Iraq, an
estimated 6% of Syrian refugee households reported
returning to Syria to seek care.15
Key evidence gaps and next steps for research
Our study shows that evidence assessing the burden of
diabetes in humanitarian settings is very limited and
generally of a low quality. Levels of need have not been
adequately captured, particularly in crises beyond the
eastern Mediterranean. The following discussion reflects
on the results of the review and proposes key research
priorities based on these findings, and our experience of
working in and researching diabetes care in crisisaffected settings (table).
Epidemiology of diabetes in humanitarian settings
There are significant knowledge gaps in the epidemiology
of diabetes in humanitarian settings, especially in Africa
and southeast Asia. Most studies were done in conflictaffected populations in the eastern Mediterranean, predominantly with refugees in host countries, rather than
in areas of conflict. Thus, further research is needed in
conflict-affected countries, particularly during the acute
phase of a crisis, and for natural disasters.
Prevalence estimates were scarce and difficult to
interpret or generalise since non-probability sampling
techniques were frequently used.57 Most studies that we
identified did not report the criteria used to diagnose or
monitor diabetes. Fingerstick glucose and HbA1c
measurements were not available or reported in most
studies. Another weakness was reporting deaths due to
diabetes, because most individuals die from complications
of diabetes rather than acute exacerbations.
Most cross-sectional surveys used self-reported medical
diagnoses that were not verified by medical reports,
which risks misdiagnoses and prevalence underestimations. For example, in a cross-sectional survey of
Palestinian households in the West Bank and Gaza Strip
that relied on self-report, 2·8% of adults had diabetes
in the West Bank and 1·9% in the Gaza Strip.21 By
contrast, the International Diabetes Federation estimated
a prevalence of 7·0% in Palestine.58 Among Syrian
refugees in Lebanon, a household telephone survey with
refugees reported a diabetes prevalence of 18%, whereas
a cross-sectional cluster survey reported a prevalence of
9·9%.18,27 Despite these differences, multiple studies
identified in this Series paper reported diabetes as one of
the top three reasons for seeking care in eastern
Mediterranean countries.15–19,27 However, the value of
these data for directing resources is questionable, given
the absence of uniform standards for data collection.
Diabetes phenotyping
The evidence we identified did not adequately capture
the various phenotypes of diabetes. Across most studies
retrieved from our search, diabetes was most often
Next steps
Burden of diabetes
Sampling techniques and outcome measures:
limited use of probabilistic sampling methods;
no uniform standards for data collection;
self-reported diagnoses not confirmed with
biochemical measurement
Develop standardised epidemiological tools and methods,
using probabilistic sampling to capture the burden of
diabetes and other NCDs during humanitarian crises;
confirm diabetes diagnoses, ideally using HbA1c
point-of-care testing
Diabetes phenotyping: prevalence and
characterisation of local diabetes epidemiology;
effective methods to rapidly identify known
cases of diabetes and other NCDs during
humanitarian crises
Strengthen surveillance and health information systems in
LMICs to improve baseline epidemiological data on diabetes
prevalence; adapt and test rapid assessment tools, which
distinguish types 1, 2, and gestational diabetes (as well as
tools for other NCDs), to map needs and available services
and to triage response in acute emergencies
Diabetes management and monitoring
Evidence-based clinical guidance on diabetes
management during crises; optimum glucose
testing method, timing, and setting; glycaemic
targets that balance safety and effectiveness;
control of cardiovascular risk factors; role of
EMRs and mHealth in clinical decision making,
self-management, and monitoring; validated
audit systems and indicators
Develop evidence-based clinical guidance on diabetes care
and cardiovascular risk reduction in crises; explore
appropriate, safe, and effective diagnostic cutoffs and
treatment targets; develop novel cost-effective
technologies for standardised glucose and cardiovascular
risk monitoring; evaluate cost-effective community or
facility-based models of diabetes care; validate indicators
and targets with a prospective study; operational research
to evaluate use of EMRs and mHealth in clinical decision
making, self-management, and monitoring
Health service use and access to care
Use of diabetes care and costs: use, access, and
coverage data for diabetes care in regions other
than the eastern Mediterranean; access to and
use of diabetes care in the acute phase of a
crisis and in natural disasters; available patient,
programmatic, and health-system costs and
cost-effective models of diabetes care in
humanitarian crises
Survey household use and access in regions other than the
eastern Mediterranean; evaluate diabetes care delivery in
the acute phase of a crisis and in natural disasters;
do descriptive studies of costs of diabetes care in
humanitarian settings from the patient and provider
perspectives; do cost-effectiveness studies of models of
care, which minimise patient direct and indirect costs
Continuity and integration of diabetes care:
effective strategies to reduce treatment
interruption in unstable settings;
evidence-based programmatic guidance on
cost-effective and sustainable integrated
primary-level delivery models, including
essential secondary prevention and referral
systems; cost-effectiveness of decentralised,
algorithm-driven care model suited to task
sharing
Develop and test emergency preparedness plans,
emergency packs, and patient-held medical records;
develop and test an algorithm-driven care model,
integrated with other NCDs, suited to task sharing,
with minimal clinical monitoring and complications
screening (potentially involving fixed-dose combination
medications); explore models of care that maximise
continuity of care and integration with other NCDs
and between different health-system levels, including
secondary prevention screening
Essential medicines and diagnostics: diabetes
essential medications and diagnostics access,
availability, and affordability; best practice and
barriers regarding insulin use in humanitarian
settings, including cold storage; role of
field-adapted point-of-care tests and technology
for diagnosis and monitoring of diabetes and
complications; effective implementation and
health-worker training around use of
Interagency Emergency Health Kit
Document diabetes essential medications and diagnostics
access, availability, and affordability in humanitarian
settings, and develop context-specific solutions, including
cold storage; field test point-of-care devices and testing
algorithms; explore novel approaches to identify and
monitor diabetes complications; evaluate Interagency
Emergency Health Kit
NCDs=non-communicable diseases. LMICs=low-income and middle-income countries. EMRs=electronic medical
records. mHealth=mobile Health.
Table: Major research gaps and proposed next steps
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reported as a single entity, and distinctions between
even the most common subtypes of diabetes (type 1,
type 2, and gestational diabetes) were rarely mentioned.
Making these distinctions is important in terms of
triage, management decisions, and resource allocation.
For example, in the acute phase of an emergency,
identifying and prioritising the care of individuals with
type 1 diabetes is crucial to minimise serious
complications and death.
Only two studies reported on the burden of gestational
diabetes.19,33 However, global estimates from 2017 suggest
that approximately 16% of total livebirths were affected by
hyperglycaemia in pregnancy, of which 88% of cases were
in LMICs.58 Gestational diabetes, which increases the
maternal risk of developing type 2 diabetes later in life, is
associated with serious adverse pregnancy outcomes, and
carries the risk of transgenerational metabolic effects on
the fetus that can be reduced through identification of
gestational diabetes and glucose control in the mother.58
Considering the volume of obstetric and perinatal care in
many humanitarian settings,3
screening and management
of hyperglycaemia in pregnancy needs to be integrated
into routine perinatal care.
Furthermore, atypical forms of diabetes have been
increasingly recognised since the 1980s. Ketosis-prone
diabetes has been recognised, mainly in populations of
African descent.59 These individuals are generally
overweight or obese and present with ketoacidosis at
diagnosis, but typically do not require long-term insulin
therapy. Lean phenotypes of diabetes, such as
malnutrition-modulated diabetes and fibrocalculous
pancreatic diabetes, are also reported mostly in
LMICs.60,61 Individuals with these forms of diabetes are
extremely lean and require high doses of insulin for
good glycaemic control; however, ketonuria rarely
occurs. Jobanputra and colleagues7
reported that staff at
a Médecins Sans Frontières-supported hospital in the
Democratic Republic of the Congo have managed
patients with type 2 diabetes, as well as those with
malnutrition-modulated diabetes who have high insulin
requirements and show signs of chronic complications
at an early stage. Thus, it is important to recognise that
individuals with diabetes might not always present in a
typical manner and, therefore, we need to improve the
characterisation of the epidemiology of diabetes in lowresource settings to identify individuals with diabetes,
particularly in protracted crises, and allocate insulin to
those who need it the most.
The dearth of baseline epidemiological data hinders
appropriate needs-assessments and response-planning,
which are essential to effectively meet the needs of crisisaffected populations. The development and standardisation of epidemiological tools and methods, particularly
digital surveillance systems, are needed to more
accurately capture the burden of diabetes (and other
NCDs) and related health needs in humanitarian
settings.
Diabetes management and monitoring
This Series paper highlights differences in treatment
targets, standards of care, and monitoring for diabetes in
humanitarian crises. Evidence-based clinical guidance on
the management and follow-up of diabetes in
humanitarian settings is not available and the
knowledge-base on cost-effective models of care in such
environments is very limited.6,7,10,11 Appropriate diagnostic
cutoffs and glycaemic targets for diabetes care in
humanitarian crises are unclear. These parameters are
particularly relevant in settings where individuals prescribed hypoglycaemic drugs are exposed to substantial
food insecurity, home-based glucose monitoring is
unavailable, and clinical follow-up is jeopardised because
of insecurity. Moreover, optimal glucose testing methods,
timing, and location in these settings are unknown.62 It is
also unclear how best to engage in secondary prevention
and screening or treatment of diabetes complications
in these settings. Importantly, data on monitoring and
control of cardiovascular risk factors in individuals with
diabetes are insufficient and need to be included in
routine diabetes care, particularly in protracted crises.
Many of these challenges also affect populations in stable
resource-poor settings. Therefore, examining diabetes
care and outcomes in crisis-affected populations compared
with those in equally resource-poor environments not
affected by a humanitarian crisis might provide helpful
insights into the unique challenges of each setting.
Available guidelines, such as the Sphere standards63
(the most widely used guidance in humanitarian crises),
provide very limited information on NCDs, including
diabetes. The WHO PEN guidelines64 provide practical
resources and information on the delivery of diabetes
care in LMICs. Although these guidelines are often used
in humanitarian crises, their effectiveness and
appropriateness in such contexts have not been studied.
The most detailed studies describing the practical
management of diabetes in humanitarian crises were
published by UNRWA.38,39,50 Screening methods, diagnostic criteria, medications, glycaemic and cardiovascular
control parameters, complications, and patient followup data were reported. Mobile phone technology was
used to contact patients to ensure follow-up and
medication adherence. Thus, there is scope to further
explore the role of electronic medical records and mobile
phone technology to support clinical decision making,
self-management, and monitoring in humanitarian
settings, and develop basic health information systems
to track patients with chronic disease over time.
Although UNRWA services for Palestinian refugees are
unique in that they serve a very long-term and relatively
static population, and cannot be generalised to more
acute crisis situations, they might provide useful
guidance.
Primary preventive and educational activities were
not addressed in any of the publications retrieved by
our search. Although these activities might not be a
644 www.thelancet.com/diabetes-endocrinology Vol 7 August 2019
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priority in the acute phase of a humanitarian response,
developing and testing cost-effective and sustainable
individual or community-based models for promotion of
self-care, adherence, and health literacy would be
valuable in protracted crisis settings.
To tackle these issues, a Working Group on NCD
control, led by UNHCR, is developing an operational
guidance document and a minimum set of NCD-specific
indicators for the management and monitoring of NCDs
across agencies. Médecins Sans Frontières has drafted
and is field-piloting a clinical guideline for NCDs during
humanitarian crisis.
Use of diabetes care and costs
This Series paper described health-care use patterns
among displaced populations with diabetes in the eastern
Mediterranean (no reports were available in other global
regions). Overall, care-seeking behaviours for individuals with diabetes and other NCDs were high. However,
access to care was substantially limited. The primary
reason for this limited access to care was the high cost of
medication and health-care services at outpatient and
inpatient facilities, fees for diagnostic evaluations,
and transportation. Each study retrieved by our search that
examined health-care access and use among displaced
populations found that high costs impeded access to
care. Medical care in camps is provided by various actors;
some might cover all costs, including medications,
laboratory tests, and referrals; others provide a minimum
package or rely on unpredictable donations of medications.
In non-camp settings, care is usually integrated within the
public health system; services are more extensive,
requiring copayments for drugs, tests, and consultations.
Thus, it is imperative to examine and implement costeffective and sustainable models of care to improve access
to care and long-term outcomes. Studies are needed to
document patient, provider, and health system costs, and
determine key cost drivers, which might be addressed
through advocacy. Cost analyses would support
humanitarian actors and host country systems in planning
for the long-term provision of expensive tests and
treatments, and specialist referral that might be required
in diabetes care. Since diabetes and its outcome are closely
linked with comorbidities, such as hypertension and
hyperlipidaemia, cost-effective models of care need to be
addressed together with other NCDs using integrated
approaches.
Continuity and integration of diabetes care
Continuity of care is a major challenge in providing care
to populations affected by humanitarian crises.6,7 None of
the studies retrieved by our search discussed ways of
dealing with this issue in unstable settings (eg, how to
ensure continuity of care when access or supplies are
compromised because of insecurity or high population
mobility). However, our search might not have captured
these studies because it was limited to quantitative studies
and these types of questions are generally explored
through qualitative research.
None of the studies described the integration of diabetes
or NCD care into host country health systems, as has
been recommended.13 Since most displaced people now
live in urban areas, rather than in camps, coordinating
and providing health-care services for these populations
is increasingly challenging.7,65 To ensure successful
response planning and delivery, developing close relationships among humanitarian organisations and
working with host country systems are important.66
Building local health system capacity in diabetes management by developing integrated NCD programmes,
establishing referral pathways, and strengthening local
supply chains, protocols, and policies will support the
delivery of diabetes care to urban-based populations and
promote sustainability post crisis. Moreover, integrating
NCD care into host country health services might be
one way to address the challenge of financing health care
in humanitarian crises, using the universal health
insurance approach.
NCD care has traditionally been provided in hospitals
and by specialists in much of the eastern Mediterranean,
with minimal involvement of primary care.67 Decentralising diabetes care to the primary care level would
allow easier access to care and follow-up, although
this decentralisation might require a substantial cultural
shift, even in stable environments. Additionally, given
the success of HIV and tuberculosis programmes that
use community health workers to deliver care in
resource-constrained settings, it is important to examine
and identify what routine tasks can be done by nonhealth professionals at the community level (eg, task
sharing of medication initiation and titration to nursing
cadres, and health education and treatment support to
community health workers).7,65 Moreover, in view of the
associations between diabetes and infectious diseases,
integrating diabetes care into the routine practice of
tuberculosis and HIV programmes would probably be
beneficial, allowing for the comanagement of NCDs and
infectious diseases that require long-term management
and close surveillance.68,69 Developing and testing
algorithm-driven, task-shared primary care models,
building on HIV and tuberculosis care experiences,
would facilitate diabetes care delivery in humanitarian
crises. Development of optimal context-adapted training
and capacity-building models in diabetes and NCD care
for humanitarian and host country health-care workers
are also needed.
Essential medicines and diagnostics
In many LMICs, the availability and continuous supply
of essential medicines is limited for people with
diabetes.70 Barriers to insulin use in LMICs include low
insulin availability, high costs, and cold storage.71,72 These
challenges are often magnified in humanitarian crises
because of insecurity, interrupted health-care systems,
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Series
population mobility, and limited coordination between
health-care providers. Diabetes medications were rarely
reported in the studies retrieved and none described
the availability or supply of medications or diagnostic
materials. Very little appears to be known about the
accessibility and af­fordability of diabetes medications
and related equipment in humanitarian crises. Documenting these access issues and developing
context-specific solutions to improve access will be
important. The use of insulin, and planning for it, in
humanitarian crises is especially complicated for the
contextual reasons given in this Series paper.
The WHO pilot of a supplemental kit to the Interagency
Emergency Health Kit, which seeks to provide a
temporary ration of medicines in humanitarian crises for
a population of 10000 people for approximately 3 months,
is a positive development.73 This kit includes metformin,
sulfonylureas, insulin, and urine and blood test strips.74
Because they are intended as temporary supplies, it is
crucial to build the capacity and resilience of local health
systems to ensure the establishment of long-term, robust
medication supply chains.75 It is also essential to include a
rapid training package to support humanitarian workers
in its implementation.
Conclusions
Our Series paper highlights that the burden of diabetes in
humanitarian crises is poorly understood, and as such,
poorly addressed. Crisis-affected populations with diabetes
face enormous constraints in accessing and receiving
care, primarily because of the high costs of care. Further
research is needed to develop standardised epidemiological
tools to better measure the burden and phenotypic
variation of diabetes in crisis-affected populations, understand access and use patterns, develop guidelines and
models of care, and evaluate their effectiveness and costeffectiveness in meeting the needs of people living with
diabetes in humanitarian crises.
Contributors
BR led the work, contributed to the literature search, contributed to
data screening and extraction, and was responsible for overall quality
control. SK finalised the search terms used, contributed to data
screening and extraction, and wrote the initial draft. JS, DCF, AC, RR,
PB, and KJ participated in data screening and extraction. EA created
the table and participated in the writing and editing of the Series paper.
PP contributed to checking and reconciling data differences, as well as
overall quality control. All authors participated in the review and
editing of the Series paper and approved the final version.
Declaration of interests
SK reports salary support from the US National Institutes of Health and
consultancy fees from Medécins Sans Frontières. EA reports grants
Search strategy and selection criteria
We searched (on Oct 30, 2017) MEDLINE, Embase, International
Bibliography of the Social Sciences, Web of Science, and Global
Health, for papers published until that date (the studies
included, as a result of the search, ranged from 1992 to 2018).
The search fields were: crisis-related terms; AND
non-communicable disease terms; AND terms related to burden,
prevalence, and incidence. The full search sources, terms, and
syntax for the published literature are provided in the appendix.
Grey literature was sought through a combination of web-based
searching of the main humanitarian databases and agency
websites and through contacting the main humanitarian
agencies doing such studies. Grey literature was updated on
Jan 29, 2018.
The population of interest was civilians (all ages) affected by
complex humanitarian crises and natural disasters in
low-income and middle-income countries (LMICs), as defined
by the World Bank. This population included refugees and
internally displaced people based on standard definitions and
those remaining in areas affected by crises. Refugees from
LMICs living in high-income countries were excluded.
Humanitarian crises were defined as events stemming from
armed conflicts, natural disasters, food insecurity, and
persecution that threaten the health and safety of a
community. The time periods of humanitarian crises included
emergency (immediate aftermath of the event up to
6 months), protracted (crisis duration >6 months), and early
recovery time periods (more stable period of rebuilding up to
2 years following the crisis). For studies that included both
crisis-affected and non-crisis-affected populations, only studies
that provided separate data for crisis and non-crisis-affected
populations were included.
The main outcome of interest was the burden of diabetes
(all types) and its complications (including fatal and non-fatal
events). The other outcomes of interest were health-care
services and access to care for individuals with diabetes.
The initial search included all non-communicable diseases
(NCDs) and from this initial literature search we included the
studies that reported data on diabetes. Mental health was not
included because it has already been reviewed elsewhere.
Studies on organ failure arising from crushes (eg, natural
disasters) were excluded. Only quantitative studies using
cross-sectional or cohort study designs (retrospective or
prospective) reporting prevalence or incidence estimates were
included. Only papers in English were included.
Study selection involved a four-stage process: removal of
duplicates (stage 1); screening by title (stage 2a) and abstract
(stage 2b), and then full text (stage 2c); grey literature
screening and review of the reference lists of the final selected
studies (stage 3); and final review and analysis of the selected
studies (stage 4). All data were double-screened and extracted
by six authors (AC, DCF, BR, JS, SK, and RR) and any variances
resolved between them. Descriptive analysis was used because
of the heterogeneous nature of study context, population
exposure, health outcomes, and study methods. Findings were
organised by the three study objectives, and then into
commonly recurring themes.
646 www.thelancet.com/diabetes-endocrinology Vol 7 August 2019
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and non-financial support from Medécins Sans Frontières. PP reports
grants from Medécins Sans Frontières. All other authors declare no
competing interests.
Acknowledgments
We thank Paul Bain (Countway Library of Medicine, Harvard Medical
School, Boston, MA, USA) for his help with the search of the scientific
literature. SK received salary support from the National Institute of
Diabetes and Digestive and Kidney Diseases of the US National
Institutes of Health (NIH; award T32DK007529). The content is solely
the responsibility of the authors and does not necessarily represent the
official views of the NIH.
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